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Two H3K23 histone methyltransferases, SET-32 and SET-21, function synergistically to promote germline nuclear RNAi, proper endogenous siRNA expression, and germline immortality in Caenorhabditis elegans [ChIP-seq]

ABSTRACT: Nuclear RNAi in C. elegans induces a set of transgenerationally heritable marks of H3K9me3, H3K23me3, and H3K27me3 at the target genes. The function of H3K23me3 in the nuclear RNAi pathway is largely unknown due to the limited knowledge of H3K23 histone methyltransferase (HMT). In this study we identified SET-21 as a novel H3K23 HMT. By taking combined genetic, biochemical, and genomic approaches we found that SET-21 functions synergistically with a previously reported H3K23 HMT SET-32 to deposit H3K23me3 at the native targets of germline nuclear RNAi. We identified a subset of nuclear RNAi targets become transcriptionally activated in the set-21;set-32 double mutant. SET-21 and SET-32 are also required for a robust transgenerational gene silencing induced by exogenous dsRNA. The loss of SET-21 and SET-32 leads to a mortal germline phenotype, similar to mutations of the core nuclear RNAi component. Together, these results support a model in which H3K23 HMTs SET-21 and SET-32 ensure the robustness of germline nuclear RNAi and promotes the germline immortality at a high temperature.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE266184 | GEO | 2024/11/01

REPOSITORIES: GEO

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Project description:Small RNA-guided chromatin silencing, also referred to as nuclear RNAi, plays an essential role in genome surveillance in eukaryotes and provides a unique paradigm to explore the complexity in RNA-mediated chromatin regulation and transgenerational epigenetics. A well-recognized paradox in this research area is that transcription of the target loci is necessary for the initiation and maintenance of the silencing at the same loci. How the two opposing activities (transcriptional activation and repression) are coordinated during animal development is poorly understood. To resolve this gap, we took single-molecule RNA imaging, deep-sequencing, and genetic approaches towards delineating the developmental regulation and subcellular localization of RNA transcripts of two exemplary endogenous germline nuclear RNAi targets in C. elegans, Cer3 and Cer8 LTR retrotransposons. By examining the wild type and a collection of mutant strains, we found that transcription and silencing cycle of Cer3 and Cer8 is tightly coupled with the early embryogenesis and germline mitotic and meiotic cell cycles. Strikingly, Cer3 and Cer8 transcripts are exclusively localized in the nuclei of germ cells in both wild type and germline nuclear RNAi-defective mutant animals. RNA-sequencing analysis found that this nuclear enrichment feature is a general feature for the endogenous targets of the germline nuclear RNAi pathway. In addition, the germline and somatic repressions of Cer3 have different genetic requirement for the three H3K9 histone methyltransferases, MET-2, SET-25, and SET-32, in conjunction with the nuclear Argonaute protein WAGO-9/HRDE-1. These results provide a first comprehensive cellular and developmental characterization of the nuclear RNAi-targeted endogenous targets throughout animal reproductive cycle. Altogether, these results support a model in which (1) both the transcriptional activation and repression steps of the germline nuclear RNAi pathway are tightly coupled with animal development, (2) the endogenous targets exhibit a hallmark of nuclear enrichment of their transcripts, and (3) different heterochromatin enzymes play distinct roles in somatic and germline silencing of the endogenous targets.

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Two H3K23 histone methyltransferases, SET-32 and SET-21, function synergistically to promote germline nuclear RNAi, proper endogenous siRNA expression, and germline immortality in Caenorhabditis elegans [ChIP-seq]

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