A novel meiotic protein required for homolog pairing and regulation of synapsis in C. elegans

Abstract

Interactions between chromosomes and LINC (Linker of Nucleoskeleton and Cytoskeleton) complexes in the nuclear envelope (NE) promote homolog pairing and synapsis during meiosis. By tethering chromosomes to cytoskeletal motors, these connections lead to rapid, processive chromosome movements along the NE. This activity is usually mediated by telomeres, but in the nematode Caenorhabditis elegans special chromosome regions called "Pairing Centers" (PCs) have acquired this meiotic function. Through a genetic screen for mutations that cause meiotic nondisjunction, we discovered an uncharacterized meiosis-specific NE protein, MJL-1 (MAJIN-Like-1) that is essential for interactions between PCs and LINC complexes. MJL-1 colocalizes with PCs and LINC complexes during pairing and synapsis. Mutations in MJL-1 disrupt these interactions and eliminate active chromosome movements. mjl-1 mutants display promiscuous nonhomologous synapsis, reduced clustering of PCs, and severely impaired homolog pairing. MJL-1 likely interacts directly with SUN-1 and DNA-binding proteins to connect PCs to the LINC complex. Similarities in the molecular architecture of chromosome-LINC complex attachments between C. elegans and other organisms suggest that these connections may play previously unrecognized roles during meiosis across eukaryotes.