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

Adél Sepsi,Trude Schwarzacher

doi:10.1242/jcs.243667

Abstract

ABSTRACTDuring 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.

Highlights

Accurate chromosome inheritance from the diploid parental cell nucleus into haploid gametes depends on the intimate juxtaposition and recombination of paternal and maternal homologous chromosomes during meiosis
Presynaptic chromatin dynamics in prophase I – progressive nuclear polarisation through centromere clustering and the telomere bouquet Before discussing chromatin dynamics during synapsis and recombination in plants, we provide a short overview of the key molecular and cytological events during various stages of meiotic prophase I, which are defined by chromosome morphology
Interpretation of 3D centromere dynamics together with immunolocalisation of the synaptonemal complex proteins in hexaploid wheat indicated that early centromere behaviour exerts a mechanistic role in homologous pairing, and defines the organisation of bulk chromatin during specific steps of synapsis and meiotic recombination (Sepsi et al, 2017)

Summary

Introduction

Accurate chromosome inheritance from the diploid parental cell nucleus into haploid gametes depends on the intimate juxtaposition and recombination of paternal and maternal homologous chromosomes (see Glossary) during meiosis. Presynaptic chromatin dynamics in prophase I – progressive nuclear polarisation through centromere clustering and the telomere bouquet Before discussing chromatin dynamics during synapsis and recombination in plants, we provide a short overview of the key molecular and cytological events during various stages of meiotic prophase I, which are defined by chromosome morphology (see definition of meiotic prophase I in Glossary; for a more-detailed discussion of early meiosis, please see recent reviews by Lambing et al, 2017; Mercier et al, 2015; Osman et al, 2011; Pradillo et al, 2014; Zickler and Kleckner, 2015). Interpretation of 3D centromere dynamics together with immunolocalisation of the synaptonemal complex proteins in hexaploid wheat indicated that early centromere behaviour exerts a mechanistic role in homologous pairing, and defines the organisation of bulk chromatin during specific steps of synapsis and meiotic recombination (Sepsi et al, 2017). Elimination of ectopic interactions – a model In this Review, we propose a model where chromatin dynamics, in tight coordination with synaptonemal complex formation, function as an effective system to eliminate ectopic interactions during plant

B Interstitial synapsis elongates from multiple points

Conclusions