Mechanisms of epigenetic regulation by C. elegans nuclear RNA interference pathways

Seroussi, Uri; Li, Chengyin; Sundby, Adam E.; Lee, Tammy L.; Claycomb, Julie M.; Saltzman, Arneet L.

doi:10.1016/j.semcdb.2021.11.018

Cited by 22 publications

(12 citation statements)

References 115 publications

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“…Epigenetic inheritance of gene expression states operates in C. elegans through small RNAs and histone modifications (Frolows & Ashe, 2021; Grishok, 2021; Ketting & Cochella, 2021; Phillips & Updike, 2022; Quarato et al , 2022; Seroussi et al , 2022). Briefly, small RNAs bound to specific Argonaute proteins enter the nucleus and induce histone modifications such as repressive H3K9me3 or H3K27 methylation at the corresponding locus, thereby silencing gene expression (Gu et al , 2012; Mao et al , 2015).…”

Section: Introductionmentioning

confidence: 99%

Genome‐wide association and environmental suppression of the mortal germline phenotype of wild C. elegans

Frézal,

Saglio,

Zhang

et al. 2023

EMBO Reports

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The animal germline lineage needs to be maintained along generations. However, some Caenorhabditis elegans wild isolates display a mortal germline phenotype, leading to sterility after several generations at 25°C. Using a genome‐wide association approach, we detect a significant peak on chromosome III around 5 Mb, confirmed by introgressions. Thus, a seemingly deleterious genotype is maintained at intermediate frequency in the species. Environmental rescue is a likely explanation, and indeed associated bacteria and microsporidia suppress the phenotype of wild isolates as well as mutants in small RNA inheritance (nrde‐2) and histone modifications (set‐2). Escherichia coli strains of the K‐12 lineage suppress the phenotype compared to B strains. By shifting a wild strain from E. coli K‐12 to E. coli B, we find that memory of the suppressing condition is maintained over several generations. Thus, the mortal germline phenotype of wild C. elegans is in part revealed by laboratory conditions and may represent variation in epigenetic inheritance and environmental interactions. This study also points to the importance of non‐genetic memory in the face of environmental variation.

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Section: Introductionmentioning

confidence: 99%

Genome‐wide association and environmental suppression of the mortal germline phenotype of wild C. elegans

Frézal,

Saglio,

Zhang

et al. 2023

EMBO Reports

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“…RNAi is a conserved mechanism of gene regulation which had been linked to chromatin modifications ( reviewed by Seroussi, 2021 ). Strinkingly, it has been proven that RNAi support epigenetic inheritance by coupling siRNAs to H3K9 methylation states in different species ( Klosin, 2017 ; Yu, 2018).…”

Section: Discussionmentioning

confidence: 99%

An environment to genome control loop using RNA interference processing of secreted tRNAs may regulates the C. elegans chemo-sensory behavior

Rémy

2022

Preprint

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Alanine tRNAs (UGC) control the development of the innate and the environment-modulated acquired C. elegans chemo-attractive responses. Some Ala-tRNA isomers are required for the development of the chemo-attractive behavior (dev-tRNAs), while others (odor-tRNAs) are made as life-term olfactory imprints of early larval odor-exposures.dev-tRNAs and odor-tRNAs biosynthesis respectively require the tRNA modifying Elongator complex sub-units ELPC-3 and ELPC-1: while elpc-3 mutants are chemo-attraction deficients, elpc-1 mutants do not synthesize odor-tRNAs imprints.Feeding wild-type dev-tRNAs restore a wild-type behavior in elpc-3 mutants. Feeding purified odor-tRNAs enhances odor responses (positive imprinting) in adult wild-type worms, while it decreases odor responses (negative imprinting) in adult imprinting deficient elpc-1 mutants.Both positive and negative imprinting can be stably inherited in worm populations. Crossing experiments indicate that both behavioral phenotypes segregate as monogenic monoallelic alterations, following Mendelian inheritance rules.Co-culture and food conditioning suggest the developmental and the odor-specific regulatory Ala-tRNAs are released in worms environment. Commensal naive acquire odor-specific imprinting from odor-experienced, while co-culture together with wild-type animals fully rescues the chemo-attractive defects of the elpc-3 mutants.Worm to worm communication of imprinting require a number of RNA interference (RNAi) genes as the intestinal RNA transporter SID-2, the initial exogenous RNAi Dicer/RDE-1/DRH-1-2/RDE-4 complexe, and the RNA-dependent RNA polymerase RRF-3. Moreover, a male contribution of the 3’-exonuclease ERI-1 activity determines whether olfactory imprints will be erased or stably fixed and inherited in worms progeny.The RNAi processing of externalized chemosensory regulatory Ala-tRNAs would generate small interfering tRNAs (si-tRNAs) able to target only tRNA complementary sequences present on worm genome, that is the tDNA genes and the transcription independent extra-TFIIIC sites.A model of control loop in which olfactory receptor expression levels in chemosensory neurons could be non-genetically but stably regulated via RNAi processing of secreted constitutive or environment-modified Ala-tRNAs is discussed.

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“…RNA interference (RNAi) is a biotechnology that inhibits the expression of specific genes; the gene interference experiments on wild-type N2 and TJ356 (zIs356 IV) nematodes were realized by introducing the pL4440 plasmid and the target genes. 24 Briefly, the pL4440 plasmid was transfected into E. coli HT115 with ampicillin (100 mg mL −1 ) through a positive cloning experiment. Worms at the L1 stage were fed with E. coli HT115 containing target genes, and after culturing to the end of the L4 larval stage, nematodes with mev-1 and isp-1 gene deletions could be obtained, and the expression of target genes mev-1 and isp-1 was analyzed by RT-PCR.…”

Section: Methodsmentioning

confidence: 99%

Mitochondria are involved in the combination of blueberry and apple peel extracts synergistically ameliorating the lifespan and oxidative stress in Caenorhabditis elegans

Song

Xia

et al. 2022

Food Funct.

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Mechanisms of epigenetic regulation by C. elegans nuclear RNA interference pathways

Cited by 22 publications

References 115 publications

Genome‐wide association and environmental suppression of the mortal germline phenotype of wild C. elegans

Genome‐wide association and environmental suppression of the mortal germline phenotype of wild C. elegans

An environment to genome control loop using RNA interference processing of secreted tRNAs may regulates the C. elegans chemo-sensory behavior

Mitochondria are involved in the combination of blueberry and apple peel extracts synergistically ameliorating the lifespan and oxidative stress in Caenorhabditis elegans

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