Meiosis reduces the number of chromosomes in reproductive cells, forming haploid gametes. It involves several cellular processes: homologous chromosome synapsis, recombination, sister-chromatid cohesion, and chromosome segregation. Members of the highly conserved SMC ( S tructural M aintenance of C hromosomes) protein family are central for diverse chromosome dynamics, including mitotic chromosome condensation and sister-chromatid cohesion as well as X-chromosome dosage compensation. We therefore explored whether SMC proteins are also involved in meiosis. Using a reverse genetic approach, we found that one C. elegans SMC protein plays a critical role in meiosis and is encoded by the
him-1 gene ( H igh I ncidence of M ales). A weak
him-1 allele causes abnormal X-chromosome nondisjunction, producing 16% males. Our results indicate that at elevated temperatures, weak
him-1 mutants have up to ten univalents at diakinesis, indicating a defect in homologous chromosome pairing. By molecular criteria,
h134 and
h55 (Rose lab) are null alleles. Maternally rescued null mutants develop into adults but are sterile with defects in germline chromosome structure, including aberrant pachytene. In wild-type animals our HIM-1 antibodies localize between homologous chromosomes during pachytene and between homologs and sister chromatids during diakinesis, further indicating a role for HIM-1 in homologous chromosome synapsis and a possible role in sister-chromatid cohesion. FISH analysis suggests that
him-1 mutants are defective in germline mitosis. Thus, SMC proteins are crucial for both mitosis and meiosis. Does
him-1 interact with dosage compensation genes involved in meiosis, such as
dpy-28 ? By immunofluorescence, DPY-28 and HIM-1 colocalize during pachytene. At diakinesis, the two antibodies show a similar staining pattern between homologs, but DPY-28 staining is greatly reduced between sister chromatids. Strikingly, DPY-28 fails to localize along meiotic chromosomes in
him-1 null mutants, indicating that it depends on HIM-1 for proper localization. In contrast, localization of DPY-28 to X during dosage compensation depends on another SMC protein, DPY-27, implying that the roles of DPY-28 in meiosis and dosage compensation are mediated by different SMC proteins.