Abstract
During meiosis, chromosomes align with their homologous pairing partners and stabilize this alignment through assembly of the synaptonemal complex (SC). Since the SC assembles cooperatively yet is indifferent to homology, pairing and SC assembly must be tightly coordinated. We identify HAL-2 as a key mediator in this coordination, showing that HAL-2 promotes pairing largely by preventing detrimental effects of SC precursors (SYP proteins). hal-2 mutants fail to establish pairing and lack multiple markers of chromosome movement mediated by pairing centers (PCs), chromosome sites that link chromosomes to cytoplasmic microtubules through nuclear envelope-spanning complexes. Moreover, SYP proteins load inappropriately along individual unpaired chromosomes in hal-2 mutants, and markers of PC-dependent movement and function are restored in hal-2; syp double mutants. These and other data indicate that SYP proteins can impede pairing and that HAL-2 promotes pairing predominantly but not exclusively by counteracting this inhibition, thereby enabling activation and regulation of PC function. HAL-2 concentrates in the germ cell nucleoplasm and colocalizes with SYP proteins in nuclear aggregates when SC assembly is prevented. We propose that HAL-2 functions to shepherd SYP proteins prior to licensing of SC assembly, preventing untimely interactions between SC precursors and chromosomes and allowing sufficient accumulation of precursors for rapid cooperative assembly upon homology verification.
Highlights
Generation of haploid gametes during sexual reproduction depends critically on the ability of homologous chromosomes to identify and form pairwise associations with their appropriate partners
We identify HAL-2, a protein that concentrates in the nucleoplasm of germ cells, as a key player in mediating this coordination
Our data suggest that HAL-2 serves to prevent inappropriate association of synaptonemal complex (SC) precursors with chromosomes prior to licensing of SC assembly, and we propose that HAL-2 may enable precursors to accumulate in a manner that allows rapid, cooperative SC assembly upon homology verification
Summary
Generation of haploid gametes during sexual reproduction depends critically on the ability of homologous chromosomes to identify and form pairwise associations with their appropriate partners. Pairing is essential to enable homologs to orient and segregate away from each other at the meiosis I division, thereby achieving the reduction in ploidy that is necessary to ensure restoration of the diploid state upon fertilization. Pairing between homologous chromosomes is reinforced by a highly ordered tripartite structure known as the synaptonemal complex (SC) that assembles at the interface between aligned homologs [1]. The lateral elements (LEs) of the SC are comprised of cohesin complexes and meiosis-specific axial components that coalesce along the length of each homolog during early meiotic prophase. SC proteins collaborate with meiosis-specific recombination proteins to promote crossover recombination events between the homologs and to promote maturation of chromosome structure surrounding crossover sites into temporary connections known as chiasmata that enable homolog segregation at the meiosis I division [2]
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