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Two parallel pathways recruit the H3K9me3 HMT in somatic cells, requiring the Argonaut NRDE-3, or the MBT-domain protein, LIN-61 (smallRNA-seq)

ABSTRACT: The establishment and maintenance of chromatin domains shape the epigenetic memory of a cell, with histone H3 lysine 9 methylation defining repressed heterochromatin. We show that in C. elegans the SET-25 (SUV39/G9a) HMT that catalyzes H3K9me1-3, is able to establish repressed domains de novo. We identify here two distinct pathways that recruit SET-25 to its targets. One requires LIN-61 (L3MBTL2), a conserved protein with 4 MBT domains that recognizes H3K9me2 deposited by the HMT MET-2 (SETDB1). The second pathway is MET-2-independent and requires a somatic Argonaut NRDE-3 and 22nt small nuclear RNAs. This NRDE-3 pathway targets ~10% of all SET-25-modified loci genome-wide including intact RNA and DNA transposons. Removal of both pathways in the met-2;nrde-3 double mutant synergistically derepresses transposons in early embryos and elevates embryonic lethality. The redundancy of these pathways illustrates the key role played by chromatin-mediated silencing in protecting the genome against inherent threats.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE156550 | GEO | 2020/12/01

REPOSITORIES: GEO

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Two parallel pathways recruit the H3K9me3 HMT in somatic cells, requiring the Argonaut NRDE-3, or the MBT-domain protein, LIN-61 (RNA-seq)

Project description:The establishment and maintenance of chromatin domains shape the epigenetic memory of a cell, with histone H3 lysine 9 methylation defining repressed heterochromatin. We show that in C. elegans the SET-25 (SUV39/G9a) HMT that catalyzes H3K9me1-3, is able to establish repressed domains de novo. We identify here two distinct pathways that recruit SET-25 to its targets. One requires LIN-61 (L3MBTL2), a conserved protein with 4 MBT domains that recognizes H3K9me2 deposited by the HMT MET-2 (SETDB1). The second pathway is MET-2-independent and requires a somatic Argonaut NRDE-3 and 22nt small nuclear RNAs. This NRDE-3 pathway targets ~10% of all SET-25-modified loci genome-wide including intact RNA and DNA transposons. Removal of both pathways in the met-2;nrde-3 double mutant synergistically derepresses transposons in early embryos and elevates embryonic lethality. The redundancy of these pathways illustrates the key role played by chromatin-mediated silencing in protecting the genome against inherent threats.

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Project description:Histone H3 lysine 9 methylation (H3K9me) and nuclear RNAi are two processes with roles in repression of repetitive elements and regulation of gene expression. Recently, they were also implicated in dosage compensation, a mechanism that accommodates for the differences in gene dosage between the biological sexes. In Caenorhabditis elegans, dosage compensation is achieved via epigenetic modifications on both X chromosomes of hermaphrodites, effectively dampening their expression by half to match the single X chromosome in males. This chromosome-wide process also relies on the anchoring and compaction of the X chromosomes near the nuclear lamina, mediated by the H3K9 histone methyltransferases MET-2, SET-25 and SET-32. H3K9me is also involved in gene silencing during nuclear RNAi, and recent evidence suggests that mutations in the nuclear RNAi machinery impact X chromosome compaction and dosage compensation. The nuclear Argonautes HRDE-1 and NRDE-3 are responsible for the recruitment of the H3K9 histone methyltransferases to targets in the germline and the soma, respectively, during nuclear RNAi. We investigated the impact of the loss of nuclear Argonautes and/or H3K9 methyltransferases on both dosage compensation and global gene expression during somatic development. Our immunofluorescence and bioinformatic analyses suggest that the nuclear RNAi and H3K9me pathways are involved in the packaging of the X chromosomes during dosage compensation, without consequence to their transcriptional output. Instead, mutant RNAi mutants exhibit global transcriptional differences, in which HRDE-1 and NRDE-3 affect expression of their native targets through different modes of regulation and different relationships between each nuclear Argonaute and H3K9 methylation.

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