Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changes
RNAs in circulation carry sequence-specific regulatory information between cells in plant, animal, and host-pathogen systems. Such RNA can cross generational boundaries, as evidenced by somatic double-stranded RNA (dsRNA) in the nematode Caenorhabditis elegans silencing genes of matching sequence in...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2025-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/99149 |
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| author | Nathan M Shugarts Devanapally Aishwarya Sathya Andrew L Yi Winnie M Chan Julia A Marre Antony M Jose |
| author_facet | Nathan M Shugarts Devanapally Aishwarya Sathya Andrew L Yi Winnie M Chan Julia A Marre Antony M Jose |
| author_sort | Nathan M Shugarts Devanapally |
| collection | DOAJ |
| description | RNAs in circulation carry sequence-specific regulatory information between cells in plant, animal, and host-pathogen systems. Such RNA can cross generational boundaries, as evidenced by somatic double-stranded RNA (dsRNA) in the nematode Caenorhabditis elegans silencing genes of matching sequence in progeny. Here we dissect the intergenerational path taken by dsRNA from parental circulation and discover that cytosolic import through the dsRNA importer SID-1 in the parental germline and/or developing progeny varies with developmental time and dsRNA substrates. Loss of SID-1 enhances initiation of heritable RNA silencing within the germline and causes changes in the expression of the sid-1-dependent gene sdg-1 that last for more than 100 generations after restoration of SID-1. The SDG-1 protein is enriched in perinuclear germ granules required for heritable RNA silencing but is expressed from a retrotransposon targeted by such silencing. This auto-inhibitory loop suggests how retrotransposons could persist by hosting genes that regulate their own silencing. |
| format | Article |
| id | doaj-art-2596155d19d241d488e06548d049fbd5 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-2596155d19d241d488e06548d049fbd52025-02-04T12:30:34ZengeLife Sciences Publications LtdeLife2050-084X2025-02-011310.7554/eLife.99149Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changesNathan M Shugarts Devanapally0https://orcid.org/0000-0003-4140-7010Aishwarya Sathya1https://orcid.org/0000-0001-6128-0040Andrew L Yi2Winnie M Chan3Julia A Marre4Antony M Jose5https://orcid.org/0000-0003-1405-0618Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, United StatesDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, United StatesDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, United StatesDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, United StatesDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, United StatesDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, United StatesRNAs in circulation carry sequence-specific regulatory information between cells in plant, animal, and host-pathogen systems. Such RNA can cross generational boundaries, as evidenced by somatic double-stranded RNA (dsRNA) in the nematode Caenorhabditis elegans silencing genes of matching sequence in progeny. Here we dissect the intergenerational path taken by dsRNA from parental circulation and discover that cytosolic import through the dsRNA importer SID-1 in the parental germline and/or developing progeny varies with developmental time and dsRNA substrates. Loss of SID-1 enhances initiation of heritable RNA silencing within the germline and causes changes in the expression of the sid-1-dependent gene sdg-1 that last for more than 100 generations after restoration of SID-1. The SDG-1 protein is enriched in perinuclear germ granules required for heritable RNA silencing but is expressed from a retrotransposon targeted by such silencing. This auto-inhibitory loop suggests how retrotransposons could persist by hosting genes that regulate their own silencing.https://elifesciences.org/articles/99149RNAitransportheritable silencingstochasticgernmlinegene expression |
| spellingShingle | Nathan M Shugarts Devanapally Aishwarya Sathya Andrew L Yi Winnie M Chan Julia A Marre Antony M Jose Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changes eLife RNAi transport heritable silencing stochastic gernmline gene expression |
| title | Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changes |
| title_full | Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changes |
| title_fullStr | Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changes |
| title_full_unstemmed | Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changes |
| title_short | Intergenerational transport of double-stranded RNA in C. elegans can limit heritable epigenetic changes |
| title_sort | intergenerational transport of double stranded rna in c elegans can limit heritable epigenetic changes |
| topic | RNAi transport heritable silencing stochastic gernmline gene expression |
| url | https://elifesciences.org/articles/99149 |
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