Histone methyltransferase MET-2 differentially regulates autosome and X-chromosome structure and transcription during...

During meiosis, accurate chromosome segregation requires significant condensation and compaction. These processes are mediated by condensins, cohesins, and histone tail modifications. We identified that MET-2, a histone methyltransferase that catalyzes the dimethylation of histone H3 lysine 9 (H3K9me2), differentially impacts chromosome size in the male vs. female C. elegans germline. In met-2 null worms, autosomes during spermatogenesis are significantly larger than wild type, while chromosome size during oogenesis is unaffected. X-univalent size in males is also unaffected by loss of MET-2, indicating MET-2 differentially regulates autosomal and X-chromosome compaction in male spermatogenesis. Autosome size is not changed when males harbor a catalytically deficient MET-2 (met-2 CD) or have mutations preventing germline histone H3K9 methylation (H3K9R). In addition, met-2 males, in contrast to met-2 CD or H3K9R males, have more active RNA pol II in later stages of meiosis. These data suggest MET-2 plays a noncatalytic role in mediating chromosome structure and transcription. In met-2 male germ lines, genes on the X chromosome, which is typically enriched in H3K9me2, are significantly more likely to be upregulated than genes on autosomes, even though X-univalent size is unchanged. These results suggest that MET-2 plays a sex-specific role that is not limited to its enzymatic activity.