Homologous chromosome pairing is a prerequisite to establish physical linkage between homologs, which is critical for faithful chromosome segregation during meiosis I. The establishment of pairing is genetically separable from subsequent synapsis, defined as stabilization of pairing by the synaptonemal complex (SC). The underlying mechanism of presynaptic pairing is poorly understood. In the nematode Caenorhabditis elegans, a unique cis-acting element, the pairing center (PC), is essential for presynaptic pairing; however, it is not known whether and how the remainder of the chromosome contributes to presynaptic pairing. Here we report direct evidence for presynaptic pairing activity intrinsic to non-PC regions, which is facilitated by a conserved chromodomain protein, MRG-1. In mrg-1 loss-of-function mutants, pairing is compromised specifically in non-PC regions, leading to nonhomologous SC assembly. Our data support a model in which presynaptic alignment in non-PC regions collaborates with initial PC pairing to ensure correct homologous synapsis.

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