Abstract
The Caenorhabditis elegans inner nuclear envelope protein matefin/SUN-1 plays a conserved, pivotal role in the process of genome haploidization. CHK-2–dependent phosphorylation of SUN-1 regulates homologous chromosome pairing and interhomolog recombination in Caenorhabditis elegans. Using time-lapse microscopy, we characterized the movement of matefin/SUN-1::GFP aggregates (the equivalent of chromosomal attachment plaques) and showed that the dynamics of matefin/SUN-1 aggregates remained unchanged throughout leptonene/zygotene, despite the progression of pairing. Movement of SUN-1 aggregates correlated with chromatin polarization. We also analyzed the requirements for the formation of movement-competent matefin/SUN-1 aggregates in the context of chromosome structure and found that chromosome axes were required to produce wild-type numbers of attachment plaques. Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement. Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics. Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.
Highlights
During the first meiotic division, homologous parental chromosomes must accomplish numerous tasks that eventually result in their connection via homologous recombination
In Caenorhabditis elegans, to find the correct pairing partner, telomere-led chromosome movement occurs in a restricted subvolume of the nucleus
Chromosomes are moved by cytoskeletal forces transmitted via the SUN/KASH bridge across the nuclear envelope, and abrogation of movement leads to precocious nonhomologous synapsis
Summary
During the first meiotic division, homologous parental chromosomes must accomplish numerous tasks that eventually result in their connection via homologous recombination. They must recognize one another, align, synapse via the tripartite proteinaceous synaptonemal complex (SC), and repair programmed double-strand breaks (DSBs); a subset of DSBs is repaired using the homologous partner as a template [1]. During this period, the chromosomes are connected to the nuclear envelope at one or both ends [2]. Interference with prophase chromosome movement in S. cerevisiae results in delayed pairing and DSB processing, aberrant crossover formation, and loss of crossover interference [6,7,11,12,13,14,15,16]
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