Genome haploidization during meiosis depends on recognition and association of parental homologous chromosomes. The C. elegans SUN/KASH domain proteins Matefin/SUN-1 and ZYG-12 have a conserved role in this process. They bridge the nuclear envelope, connecting the cytoplasm and the nucleoplasm to transmit forces that allow chromosome movement and homolog pairing and prevent nonhomologous synapsis. Here, we show that Matefin/SUN-1 forms rapidly moving aggregates at putative chromosomal attachment sites in the meiotic transition zone (TZ). We analyzed requirements for aggregate formation and identified multiple phosphotarget residues in the nucleoplasmic domain of Matefin/SUN-1. These CHK-2 dependent phosphorylations occur in leptotene/zygotene, diminish during pachytene and are involved in pairing. Mimicking phosphorylation causes an extended TZ and univalents at diakinesis. Our data suggest that the properties of the nuclear envelope are altered during the time window when homologs are sorted and Matefin/SUN-1 aggregates form, thereby controling the movement, homologous pairing and interhomolog recombination of chromosomes.
We identify a highly specific mutation (jf18) in the Caenorhabditis elegans nuclear envelope protein matefin MTF-1/SUN-1 that provides direct evidence for active involvement of the nuclear envelope in homologous chromosome pairing in C. elegans meiosis. The reorganization of chromatin in early meiosis is disrupted in mtf-1/sun-1(jf18) gonads, concomitant with the absence of presynaptic homolog alignment. Synapsis is established precociously and nonhomologously. Wild-type leptotene/zygotene nuclei show patch-like aggregations of the ZYG-12 protein, which fail to develop in mtf-1/sun-1(jf18) mutants. These patches remarkably colocalize with a component of the cis-acting chromosomal pairing center (HIM-8) rather than the centrosome. Our data on this mtf-1/sun-1 allele challenge the previously postulated role of the centrosome/spindle organizing center in chromosome pairing, and clearly support a role for MTF-1/SUN-1 in meiotic chromosome reorganization and in homolog recognition, possibly by mediating local aggregation of the ZYG-12 protein in meiotic nuclei.
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