Segregation of homologous chromosomes is the landmark event of meiosis. This essential feature relies on the coordinated execution of a complex set of interconnected events: homologous chromosomes must first locate, recognize and align with their correct pairing partners during a period of active chromosome movement. This alignment is stabilized through the assembly of a meiosis-specific structure known as the synaptonemal complex (SC), which promotes formation of crossover recombination events between the DNA molecules of the homologs to create the linkages that enable their segregation. Here, we identify HAL-3 (Homolog Alignment 3), as a partner of the nucleoplasmic protein HAL-2 previously described as an important regulator of early prophase events in the model organism C. elegans (Zhang et al., 2012). We show that loss of
hal-3 function phenocopies multiple defects observed in
hal-2 mutant meiocytes, including failure to establish homolog pairing and inappropriate loading of SC subunits onto unpaired chromosome axes. Proper coordingation between homolog pairing and synapsis is ensured, in part, by the activity of the polo-like kinases PLK-1 and PLK-2, which dynamically localize at defined subnuclear locations during wild-type prophase progression. We show that loss of hal function results in misregulation of the subcellular localization of PLK-1 and PLK-2, and we provide evidence for PLK activity at ectopic locations in
hal-2 and
hal-3 mutants. Further, we find that loss of PLK-2 activity partially suppresses several meiotic defects in hal mutants, suggesting that the defects result from inappropriate PLK activity. Together our data support a model in which the nucleoplasmic HAL-2/HAL-3 complex regulates early meiotic prophase events by constraining both localization and activity of meiotic Polo-like kinases, both to prevent interaction with untimely targets and to promote proper association with stage-appropriate targets.