Meiotic H3K9me2 distribution is influenced by the ALG-3 and ALG-4 pathway and by poly(U) polymerase activity

Histone modifications influence gene expression and chromosome dynamics by altering chromatin structure and recruitment of nonhistone proteins. Dimethylation of histone H3 on lysine 9 (H3K9me2) is a conserved modification often found within heterochromatin. During first meiotic prophase when homologous chromosomes undergo pairing and synapsis, immunolabeling of C. elegans male germ cells detects a relatively high H3K9me2 level on the single X chromosome and a relatively low H3K9me2 level on synapsed autosomes. This H3K9me2 distribution is influenced by several components of the small RNA machinery, including: EGO-1 RNA-directed RNA polymerase (RdRP); DRH-3 helicase; EKL-1, a Tudor domain protein; CSR-1 Argonaute; and RRF-3 RdRP. EGO-1, DRH-3, and EKL-1 function together to generate/stabilize 22G RNAs in the germ line. A subset of these 22G RNAs function together with CSR-1 to ensure correct gene expression. RRF-3 RdRP functions in biogenesis of 26G RNAs that feed into two germline regulatory mechanisms mediated by ERGO-1 Argonaute and the redundant ALG-3 and ALG-4 Argonaute proteins. Here, we report that meiotic H3K9me2 distribution is influenced by ALG-3 and ALG-4, as well as by two other factors required for 26G RNA synthesis, ERI-1 and ERI-5. Moreover, meiotic H3K9me2 distribution is influenced by activity of the poly(U) polymerases, PUP-1 (aka CDE-1, CID-1) and PUP-2.