{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,28]],"date-time":"2026-10-28T15:56:48Z","timestamp":1793203008436,"version":"4.5.0"},"reference-count":78,"publisher":"Springer Science and Business Media LLC","issue":"8006","license":[{"start":{"date-parts":[[2024,3,6]],"date-time":"2024-03-06T00:00:00Z","timestamp":1709683200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,3,6]],"date-time":"2024-03-06T00:00:00Z","timestamp":1709683200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nature"],"published-print":{"date-parts":[[2024,4,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Genomic imprinting\u2014the non-equivalence of maternal and paternal genomes\u2014is a critical process that has evolved independently in many plant and mammalian species<jats:sup>1,2<\/jats:sup>. According to kinship theory, imprinting is the inevitable consequence of conflictive selective forces acting on differentially expressed parental alleles<jats:sup>3,4<\/jats:sup>. Yet, how these epigenetic differences evolve in the first place is poorly understood<jats:sup>3,5,6<\/jats:sup>. Here we report the identification and molecular dissection of a parent-of-origin effect on gene expression that might help to clarify this fundamental question. Toxin-antidote elements (TAs) are selfish elements that spread in populations by poisoning non-carrier individuals<jats:sup>7\u20139<\/jats:sup>. In reciprocal crosses between two <jats:italic>Caenorhabditis tropicalis<\/jats:italic> wild isolates, we found that the <jats:italic>slow-1\/grow-1<\/jats:italic> TA is specifically inactive when paternally inherited. This parent-of-origin effect stems from transcriptional repression of the <jats:italic>slow-1<\/jats:italic> toxin by the PIWI-interacting RNA (piRNA) host defence pathway. The repression requires PIWI Argonaute and SET-32 histone methyltransferase activities and is transgenerationally inherited via small RNAs. Remarkably, when <jats:italic>slow-1\/grow-1<\/jats:italic> is maternally inherited, <jats:italic>slow-1<\/jats:italic> repression is halted by a translation-independent role of its maternal mRNA. That is, <jats:italic>slow-1<\/jats:italic> transcripts loaded into eggs\u2014but not SLOW-1 protein\u2014are necessary and sufficient to counteract piRNA-mediated repression. Our findings show that parent-of-origin effects can evolve by co-option of the piRNA pathway and hinder the spread of selfish genes that require sex for their propagation.<\/jats:p>","DOI":"10.1038\/s41586-024-07155-z","type":"journal-article","created":{"date-parts":[[2024,3,6]],"date-time":"2024-03-06T17:02:35Z","timestamp":1709744555000},"page":"122-129","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["Selfish conflict underlies RNA-mediated parent-of-origin effects"],"prefix":"10.1038","volume":"628","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1406-5978","authenticated-orcid":false,"given":"Pinelopi","family":"Pliota","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hana","family":"Marvanova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5661-8577","authenticated-orcid":false,"given":"Alevtina","family":"Koreshova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yotam","family":"Kaufman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Polina","family":"Tikanova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4535-7540","authenticated-orcid":false,"given":"Daniel","family":"Krogull","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreas","family":"Hagm\u00fcller","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7224-2701","authenticated-orcid":false,"given":"Sonya A.","family":"Widen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1059-4960","authenticated-orcid":false,"given":"Dominik","family":"Handler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph","family":"Gokcezade","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Duchek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5141-0814","authenticated-orcid":false,"given":"Julius","family":"Brennecke","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0514-0400","authenticated-orcid":false,"given":"Eyal","family":"Ben-David","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0211-4357","authenticated-orcid":false,"given":"Alejandro","family":"Burga","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,3,6]]},"reference":[{"key":"7155_CR1","doi-asserted-by":"crossref","first-page":"a018382","DOI":"10.1101\/cshperspect.a018382","volume":"6","author":"DP Barlow","year":"2014","unstructured":"Barlow, D. P. & Bartolomei, M. S. Genomic imprinting in mammals. Cold Spring Harb. Perspect. Biol. 6, a018382 (2014).","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"7155_CR2","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/35047554","volume":"2","author":"W Reik","year":"2001","unstructured":"Reik, W. & Walter, J. Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21\u201332 (2001).","journal-title":"Nat. Rev. Genet."},{"key":"7155_CR3","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1146\/annurev.ecolsys.31.1.9","volume":"31","author":"D Haig","year":"2000","unstructured":"Haig, D. The kinship theory of genomic imprinting. Annu. Rev. Ecol. Syst. 31, 9\u201332 (2000).","journal-title":"Annu. Rev. Ecol. Syst."},{"key":"7155_CR4","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/0168-9525(91)90040-W","volume":"7","author":"T Moore","year":"1991","unstructured":"Moore, T. & Haig, D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 7, 45\u201349 (1991).","journal-title":"Trends Genet."},{"key":"7155_CR5","doi-asserted-by":"crossref","first-page":"e1008599","DOI":"10.1371\/journal.pgen.1008599","volume":"16","author":"M Ondi\u010dov\u00e1","year":"2020","unstructured":"Ondi\u010dov\u00e1, M., Oakey, R. J. & Walsh, C. P. Is imprinting the result of \u201cfriendly fire\u201d by the host defense system? PLoS Genet. 16, e1008599 (2020).","journal-title":"PLoS Genet."},{"key":"7155_CR6","doi-asserted-by":"crossref","unstructured":"Burt, A. & Trivers, R. Genes in Conflict: The Biology of Selfish Genetic Elements (Harvard University Press, 2006).","DOI":"10.4159\/9780674029118"},{"key":"7155_CR7","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1146\/annurev-genet-112618-043659","volume":"54","author":"A Burga","year":"2020","unstructured":"Burga, A., Ben-David, E. & Kruglyak, L. Toxin\u2013antidote elements across the Tree of Life. Annu. Rev. Genet. 54, 387\u2013415 (2020).","journal-title":"Annu. Rev. Genet."},{"key":"7155_CR8","doi-asserted-by":"crossref","first-page":"1051","DOI":"10.1126\/science.aan0621","volume":"356","author":"E Ben-David","year":"2017","unstructured":"Ben-David, E., Burga, A. & Kruglyak, L. A maternal-effect selfish genetic element in Caenorhabditis elegans. Science 356, 1051\u20131055 (2017).","journal-title":"Science"},{"key":"7155_CR9","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1016\/j.cub.2020.12.013","volume":"31","author":"E Ben-David","year":"2021","unstructured":"Ben-David, E. et al. Ubiquitous selfish toxin\u2013antidote elements in Caenorhabditis species. Curr. Biol. 31, 990\u20131001.e5 (2021).","journal-title":"Curr. Biol."},{"key":"7155_CR10","doi-asserted-by":"crossref","first-page":"352","DOI":"10.1038\/s41477-018-0161-6","volume":"4","author":"C Lafon-Placette","year":"2018","unstructured":"Lafon-Placette, C. et al. Paternally expressed imprinted genes associate with hybridization barriers in Capsella. Nat. Plants 4, 352\u2013357 (2018).","journal-title":"Nat. Plants"},{"key":"7155_CR11","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1126\/science.8469984","volume":"260","author":"DP Barlow","year":"1993","unstructured":"Barlow, D. P. Methylation and imprinting: from host defense to gene regulation? Science 260, 309\u2013310 (1993).","journal-title":"Science"},{"key":"7155_CR12","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1038\/366362a0","volume":"366","author":"E Li","year":"1993","unstructured":"Li, E., Beard, C. & Jaenisch, R. Role for DNA methylation in genomic imprinting. Nature 366, 362\u2013365 (1993).","journal-title":"Nature"},{"key":"7155_CR13","doi-asserted-by":"crossref","first-page":"e03198","DOI":"10.7554\/eLife.03198","volume":"3","author":"D Pignatta","year":"2014","unstructured":"Pignatta, D. et al. Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting. eLife 3, e03198 (2014).","journal-title":"eLife"},{"key":"7155_CR14","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1146\/annurev-genet-110711-155527","volume":"47","author":"M Gehring","year":"2013","unstructured":"Gehring, M. Genomic imprinting: insights from plants. Annu. Rev. Genet. 47, 187\u2013208 (2013).","journal-title":"Annu. Rev. Genet."},{"key":"7155_CR15","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1126\/science.1203919","volume":"332","author":"T Watanabe","year":"2011","unstructured":"Watanabe, T. et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332, 848\u2013852 (2011).","journal-title":"Science"},{"key":"7155_CR16","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1038\/nature23262","volume":"547","author":"A Inoue","year":"2017","unstructured":"Inoue, A., Jiang, L., Lu, F., Suzuki, T. & Zhang, Y. Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature 547, 419\u2013424 (2017).","journal-title":"Nature"},{"key":"7155_CR17","doi-asserted-by":"crossref","first-page":"416","DOI":"10.3389\/fgene.2014.00416","volume":"5","author":"EM Youngman","year":"2014","unstructured":"Youngman, E. M. & Claycomb, J. M. From early lessons to new frontiers: the worm as a treasure trove of small RNA biology. Front. Genet. 5, 416 (2014).","journal-title":"Front. Genet."},{"key":"7155_CR18","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1186\/1471-2148-11-339","volume":"11","author":"KC Kiontke","year":"2011","unstructured":"Kiontke, K. C. et al. A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol. Biol. 11, 339 (2011).","journal-title":"BMC Evol. Biol."},{"key":"7155_CR19","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1126\/science.1151107","volume":"319","author":"HS Seidel","year":"2008","unstructured":"Seidel, H. S., Rockman, M. V. & Kruglyak, L. Widespread genetic incompatibility in C. elegans maintained by balancing selection. Science 319, 589\u2013594 (2008).","journal-title":"Science"},{"key":"7155_CR20","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1126\/science.1566060","volume":"256","author":"RW Beeman","year":"1992","unstructured":"Beeman, R. W., Friesen, K. S. & Denell, R. E. Maternal-effect selfish genes in flour beetles. Science 256, 89\u201392 (1992).","journal-title":"Science"},{"key":"7155_CR21","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1017\/S0016672300034017","volume":"68","author":"D Weichenhan","year":"1996","unstructured":"Weichenhan, D., Traut, W., Kunze, B. & Winking, H. Distortion of Mendelian recovery ratio for a mouse HSR is caused by maternal and zygotic effects. Genet. Res. 68, 125\u2013129 (1996).","journal-title":"Genet. Res."},{"key":"7155_CR22","doi-asserted-by":"crossref","first-page":"eade0705","DOI":"10.1126\/science.ade0705","volume":"380","author":"SA Widen","year":"2023","unstructured":"Widen, S. A. et al. Virus-like transposons cross the species barrier and drive the evolution of genetic incompatibilities. Science 380, eade0705 (2023).","journal-title":"Science"},{"key":"7155_CR23","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1038\/s41588-018-0061-8","volume":"50","author":"S Ro\u0161i\u0107","year":"2018","unstructured":"Ro\u0161i\u0107, S. et al. Evolutionary analysis indicates that DNA alkylation damage is a byproduct of cytosine DNA methyltransferase activity. Nat. Genet. 50, 452\u2013459 (2018).","journal-title":"Nat. Genet."},{"key":"7155_CR24","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1534\/genetics.104.040303","volume":"170","author":"K Sha","year":"2005","unstructured":"Sha, K. & Fire, A. Imprinting capacity of gamete lineages in Caenorhabditis elegans. Genetics 170, 1633\u20131652 (2005).","journal-title":"Genetics"},{"key":"7155_CR25","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-021-24053-4","volume":"12","author":"S Devanapally","year":"2021","unstructured":"Devanapally, S. et al. Mating can initiate stable RNA silencing that overcomes epigenetic recovery. Nat. Commun. 12, 4239 (2021).","journal-title":"Nat. Commun."},{"key":"7155_CR26","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1534\/genetics.108.089433","volume":"180","author":"RM Alcazar","year":"2008","unstructured":"Alcazar, R. M., Lin, R. & Fire, A. Z. Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans. Genetics 180, 1275\u20131288 (2008).","journal-title":"Genetics"},{"key":"7155_CR27","doi-asserted-by":"crossref","first-page":"1186","DOI":"10.1016\/j.cell.2020.07.022","volume":"182","author":"L Houri-Zeevi","year":"2020","unstructured":"Houri-Zeevi, L., Korem Kohanim, Y., Antonova, O. & Rechavi, O. Three rules explain transgenerational small rna inheritance in C. elegans. Cell 182, 1186\u20131197.e12 (2020).","journal-title":"Cell"},{"key":"7155_CR28","doi-asserted-by":"crossref","first-page":"1827","DOI":"10.1016\/j.cell.2019.05.024","volume":"177","author":"RS Moore","year":"2019","unstructured":"Moore, R. S., Kaletsky, R. & Murphy, C. T. Piwi\/PRG-1 Argonaute and TGF-\u03b2 mediate transgenerational learned pathogenic avoidance. Cell 177, 1827\u20131841.e12 (2019).","journal-title":"Cell"},{"key":"7155_CR29","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1126\/science.1220952","volume":"337","author":"MP Bagijn","year":"2012","unstructured":"Bagijn, M. P. et al. Function, targets, and evolution of Caenorhabditis elegans piRNAs. Science 337, 574\u2013578 (2012).","journal-title":"Science"},{"key":"7155_CR30","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.molcel.2008.06.002","volume":"31","author":"PJ Batista","year":"2008","unstructured":"Batista, P. J. et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell 31, 67\u201378 (2008).","journal-title":"Mol. Cell"},{"key":"7155_CR31","doi-asserted-by":"crossref","first-page":"3422","DOI":"10.1038\/emboj.2012.213","volume":"31","author":"MJ Luteijn","year":"2012","unstructured":"Luteijn, M. J. et al. Extremely stable Piwi-induced gene silencing in Caenorhabditis elegans. EMBO J. 31, 3422\u20133430 (2012).","journal-title":"EMBO J."},{"key":"7155_CR32","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.cell.2012.06.015","volume":"150","author":"M Shirayama","year":"2012","unstructured":"Shirayama, M. et al. piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 150, 65\u201377 (2012).","journal-title":"Cell"},{"key":"7155_CR33","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1016\/j.cell.2006.10.040","volume":"127","author":"JG Ruby","year":"2006","unstructured":"Ruby, J. G. et al. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127, 1193\u20131207 (2006).","journal-title":"Cell"},{"key":"7155_CR34","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1038\/nature11352","volume":"489","author":"BA Buckley","year":"2012","unstructured":"Buckley, B. A. et al. A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. Nature 489, 447\u2013451 (2012).","journal-title":"Nature"},{"key":"7155_CR35","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.cell.2012.06.018","volume":"150","author":"A Ashe","year":"2012","unstructured":"Ashe, A. et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150, 88\u201399 (2012).","journal-title":"Cell"},{"key":"7155_CR36","doi-asserted-by":"crossref","first-page":"e54309","DOI":"10.7554\/eLife.54309","volume":"9","author":"L Schwartz-Orbach","year":"2020","unstructured":"Schwartz-Orbach, L. et al. Caenorhabditis elegans nuclear RNAi factor SET-32 deposits the transgenerational histone modification, H3K23me3. eLife 9, e54309 (2020).","journal-title":"eLife"},{"key":"7155_CR37","doi-asserted-by":"crossref","first-page":"e1005078","DOI":"10.1371\/journal.pgen.1005078","volume":"11","author":"A Sapetschnig","year":"2015","unstructured":"Sapetschnig, A., Sarkies, P., Lehrbach, N. J. & Miska, E. A. Tertiary siRNAs mediate paramutation in C. elegans. PLoS Genet. 11, e1005078 (2015).","journal-title":"PLoS Genet."},{"key":"7155_CR38","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/s13072-017-0114-8","volume":"10","author":"N Kalinava","year":"2017","unstructured":"Kalinava, N., Ni, J. Z., Peterman, K., Chen, E. & Gu, S. G. Decoupling the downstream effects of germline nuclear RNAi reveals that H3K9me3 is dispensable for heritable RNAi and the maintenance of endogenous siRNA-mediated transcriptional silencing in Caenorhabditis elegans. Epigenet. Chromatin 10, 6 (2017).","journal-title":"Epigenet. Chromatin"},{"key":"7155_CR39","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1038\/ng.1039","volume":"44","author":"SG Gu","year":"2012","unstructured":"Gu, S. G. et al. Amplification of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint. Nat. Genet. 44, 157\u2013164 (2012).","journal-title":"Nat. Genet."},{"key":"7155_CR40","doi-asserted-by":"crossref","first-page":"2273","DOI":"10.1016\/j.celrep.2018.10.086","volume":"25","author":"N Kalinava","year":"2018","unstructured":"Kalinava, N. et al. C. elegans heterochromatin factor SET-32 plays an essential role in transgenerational establishment of nuclear RNAi-mediated epigenetic silencing. Cell Rep. 25, 2273\u20132284.e3 (2018).","journal-title":"Cell Rep."},{"key":"7155_CR41","doi-asserted-by":"crossref","first-page":"2259","DOI":"10.1016\/j.celrep.2018.10.085","volume":"25","author":"RM Woodhouse","year":"2018","unstructured":"Woodhouse, R. M. et al. Chromatin modifiers SET-25 and SET-32 are required for establishment but not long-term maintenance of transgenerational epigenetic inheritance. Cell Rep. 25, 2259\u20132272.e5 (2018).","journal-title":"Cell Rep."},{"key":"7155_CR42","doi-asserted-by":"crossref","first-page":"e40448","DOI":"10.7554\/eLife.40448","volume":"8","author":"I Lev","year":"2019","unstructured":"Lev, I., Gingold, H. & Rechavi, O. H3K9me3 is required for inheritance of small RNAs that target a unique subset of newly evolved genes. eLife 8, e40448 (2019).","journal-title":"eLife"},{"key":"7155_CR43","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1534\/genetics.106.057364","volume":"173","author":"A Fire","year":"2006","unstructured":"Fire, A., Alcazar, R. & Tan, F. Unusual DNA structures associated with germline genetic activity in Caenorhabditis elegans. Genetics 173, 1259\u20131273 (2006).","journal-title":"Genetics"},{"key":"7155_CR44","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1016\/j.cell.2016.05.072","volume":"166","author":"C Fr\u00f8kj\u00e6r-Jensen","year":"2016","unstructured":"Fr\u00f8kj\u00e6r-Jensen, C. et al. An abundant class of non-coding DNA can prevent stochastic gene silencing in the C. elegans germline. Cell 166, 343\u2013357 (2016).","journal-title":"Cell"},{"key":"7155_CR45","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1126\/science.1208178","volume":"333","author":"CL Johnson","year":"2011","unstructured":"Johnson, C. L. & Spence, A. M. Epigenetic licensing of germline gene expression by maternal RNA in C. elegans. Science 333, 1311\u20131314 (2011).","journal-title":"Science"},{"key":"7155_CR46","doi-asserted-by":"crossref","first-page":"dev200692","DOI":"10.1242\/dev.200692","volume":"149","author":"Z Gajic","year":"2022","unstructured":"Gajic, Z. et al. Target-dependent suppression of siRNA production modulates the levels of endogenous siRNAs in the Caenorhabditis elegans germline. Development 149, dev200692 (2022).","journal-title":"Development"},{"key":"7155_CR47","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1038\/nrg995","volume":"4","author":"T Blumenthal","year":"2003","unstructured":"Blumenthal, T. & Gleason, K. S. Caenorhabditis elegans operons: form and function. Nat. Rev. Genet. 4, 110\u2013118 (2003).","journal-title":"Nat. Rev. Genet."},{"key":"7155_CR48","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/0092-8674(93)90139-H","volume":"73","author":"J Spieth","year":"1993","unstructured":"Spieth, J., Brooke, G., Kuersten, S., Lea, K. & Blumenthal, T. Operons in C. elegans: polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions. Cell 73, 521\u2013532 (1993).","journal-title":"Cell"},{"key":"7155_CR49","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.molcel.2009.09.020","volume":"36","author":"W Gu","year":"2009","unstructured":"Gu, W. et al. Distinct Argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol. Cell 36, 231\u2013244 (2009).","journal-title":"Mol. Cell"},{"key":"7155_CR50","doi-asserted-by":"crossref","first-page":"1532","DOI":"10.1016\/j.cell.2013.11.032","volume":"155","author":"CC Conine","year":"2013","unstructured":"Conine, C. C. et al. Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans. Cell 155, 1532\u20131544 (2013).","journal-title":"Cell"},{"key":"7155_CR51","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1126\/science.aar4279","volume":"360","author":"X Yu","year":"2018","unstructured":"Yu, X. et al. A selfish genetic element confers non-Mendelian inheritance in rice. Science 360, 1130\u20131132 (2018).","journal-title":"Science"},{"key":"7155_CR52","doi-asserted-by":"crossref","first-page":"11436","DOI":"10.1073\/pnas.0804761105","volume":"105","author":"J Chen","year":"2008","unstructured":"Chen, J. et al. A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica\u2013japonica hybrids in rice. Proc. Natl Acad. Sci. USA 105, 11436\u201311441 (2008).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"7155_CR53","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1534\/genetics.120.303564","volume":"216","author":"KS Ghanta","year":"2020","unstructured":"Ghanta, K. S. & Mello, C. C. Melting dsDNA donor molecules greatly improves precision genome editing in Caenorhabditis elegans. Genetics 216, 643\u2013650 (2020).","journal-title":"Genetics"},{"key":"7155_CR54","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1038\/s41587-019-0072-8","volume":"37","author":"M Kolmogorov","year":"2019","unstructured":"Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540\u2013546 (2019).","journal-title":"Nat. Biotechnol."},{"key":"7155_CR55","doi-asserted-by":"crossref","unstructured":"Minkin, I., Patel, A., Kolmogorov, M., Vyahhi, N. & Pham, S. in Algorithms in Bioinformatics (eds Darling, A. & Stoye, J.) 215\u2013229 (Springer, 2013).","DOI":"10.1007\/978-3-642-40453-5_17"},{"key":"7155_CR56","doi-asserted-by":"crossref","first-page":"i302","DOI":"10.1093\/bioinformatics\/btu280","volume":"30","author":"M Kolmogorov","year":"2014","unstructured":"Kolmogorov, M., Raney, B., Paten, B. & Pham, S. Ragout\u2014a reference-assisted assembly tool for bacterial genomes. Bioinformatics 30, i302\u2013i309 (2014).","journal-title":"Bioinformatics"},{"key":"7155_CR57","doi-asserted-by":"crossref","first-page":"e83853","DOI":"10.7554\/eLife.83853","volume":"12","author":"U Seroussi","year":"2023","unstructured":"Seroussi, U. et al. A comprehensive survey of C. elegans argonaute proteins reveals organism-wide gene regulatory networks and functions. eLife 12, e83853 (2023).","journal-title":"eLife"},{"key":"7155_CR58","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1093\/molbev\/msaa015","volume":"37","author":"BQ Minh","year":"2020","unstructured":"Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530\u20131534 (2020).","journal-title":"Mol. Biol. Evol."},{"key":"7155_CR59","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.molbiopara.2016.11.005","volume":"215","author":"KL Howe","year":"2017","unstructured":"Howe, K. L., Bolt, B. J., Shafie, M., Kersey, P. & Berriman, M. WormBase ParaSite\u2014a comprehensive resource for helminth genomics. Mol. Biochem. Parasitol. 215, 2\u201310 (2017).","journal-title":"Mol. Biochem. Parasitol."},{"key":"7155_CR60","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","volume":"596","author":"J Jumper","year":"2021","unstructured":"Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583\u2013589 (2021).","journal-title":"Nature"},{"key":"7155_CR61","doi-asserted-by":"publisher","unstructured":"van Kempen, M. et al. Fast and accurate protein structure search with Foldseek. Nat. Biotechnol. https:\/\/doi.org\/10.1038\/s41587-023-01773-0 (2023).","DOI":"10.1038\/s41587-023-01773-0"},{"key":"7155_CR62","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/978-1-4939-3578-9_16","volume":"1418","author":"F Hahne","year":"2016","unstructured":"Hahne, F. & Ivanek, R. Visualizing genomic data using Gviz and Bioconductor. Stat. Genomics 1418, 335\u2013351 (2016).","journal-title":"Stat. Genomics"},{"key":"7155_CR63","doi-asserted-by":"crossref","DOI":"10.1186\/1748-7188-6-26","volume":"6","author":"R Lorenz","year":"2011","unstructured":"Lorenz, R. et al. ViennaRNA package 2.0. Algorithms for Mol. Biol. 6, 26 (2011).","journal-title":"Algorithms for Mol. Biol."},{"key":"7155_CR64","volume":"15","author":"JZ Ni","year":"2014","unstructured":"Ni, J. Z., Chen, E. & Gu, S. G. Complex coding of endogenous siRNA, transcriptional silencing and H3K9 methylation on native targets of germline nuclear RNAi in C. elegans. BMC Genomics 15, 1157 (2014).","journal-title":"BMC Genomics"},{"key":"7155_CR65","unstructured":"Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https:\/\/arxiv.org\/abs\/1303.3997 (2013)."},{"key":"7155_CR66","unstructured":"Green, M. R. & Sambrook, J. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 2012)."},{"key":"7155_CR67","doi-asserted-by":"crossref","DOI":"10.1186\/1471-2199-9-9","volume":"9","author":"D Hoogewijs","year":"2008","unstructured":"Hoogewijs, D., Houthoofd, K., Matthijssens, F., Vandesompele, J. & Vanfleteren, J. R. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol. Biol. 9, 9 (2008).","journal-title":"BMC Mol. Biol."},{"key":"7155_CR68","doi-asserted-by":"crossref","first-page":"e50014","DOI":"10.7554\/eLife.50014","volume":"9","author":"V Serobyan","year":"2020","unstructured":"Serobyan, V. et al. Transcriptional adaptation in Caenorhabditis elegans. eLife 9, e50014 (2020).","journal-title":"eLife"},{"key":"7155_CR69","doi-asserted-by":"crossref","first-page":"e79","DOI":"10.1093\/nar\/gkaa472","volume":"48","author":"T Grentzinger","year":"2020","unstructured":"Grentzinger, T. et al. A universal method for the rapid isolation of all known classes of functional silencing small RNAs. Nucleic Acids Res. 48, e79 (2020).","journal-title":"Nucleic Acids Res."},{"key":"7155_CR70","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.mex.2019.01.009","volume":"6","author":"MV Almeida","year":"2019","unstructured":"Almeida, M. V., de Jesus Domingues, A. M., Lukas, H., Mendez-Lago, M. & Ketting, R. F. RppH can faithfully replace TAP to allow cloning of 5\u2032-triphosphate carrying small RNAs. MethodsX 6, 265\u2013272 (2019).","journal-title":"MethodsX"},{"key":"7155_CR71","doi-asserted-by":"crossref","first-page":"10","DOI":"10.14806\/ej.17.1.200","volume":"17","author":"M Martin","year":"2011","unstructured":"Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10\u201312 (2011).","journal-title":"EMBnet.journal"},{"key":"7155_CR72","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","volume":"37","author":"D Kim","year":"2019","unstructured":"Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907\u2013915 (2019).","journal-title":"Nat. Biotechnol."},{"key":"7155_CR73","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","volume":"25","author":"H Li","year":"2009","unstructured":"Li, H. et al. The Sequence Alignment\/Map format and SAMtools. Bioinformatics 25, 2078\u20132079 (2009).","journal-title":"Bioinformatics"},{"key":"7155_CR74","volume":"9","author":"Y Zhang","year":"2008","unstructured":"Zhang, Y. et al. Model-based Analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).","journal-title":"Genome Biol."},{"key":"7155_CR75","doi-asserted-by":"crossref","first-page":"W160","DOI":"10.1093\/nar\/gkw257","volume":"44","author":"F Ram\u00edrez","year":"2016","unstructured":"Ram\u00edrez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160\u2013W165 (2016).","journal-title":"Nucleic Acids Res."},{"key":"7155_CR76","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","volume":"26","author":"AR Quinlan","year":"2010","unstructured":"Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841\u2013842 (2010).","journal-title":"Bioinformatics"},{"key":"7155_CR77","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","volume":"9","author":"J Schindelin","year":"2012","unstructured":"Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676\u2013682 (2012).","journal-title":"Nat. Methods"},{"key":"7155_CR78","doi-asserted-by":"crossref","first-page":"dev174029","DOI":"10.1242\/dev.174029","volume":"146","author":"S Wang","year":"2019","unstructured":"Wang, S. et al. A high-content imaging approach to profile C. elegans embryonic development. Development 146, dev174029 (2019).","journal-title":"Development"}],"container-title":["Nature"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07155-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07155-z","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07155-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,7]],"date-time":"2024-04-07T02:02:31Z","timestamp":1712455351000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07155-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,6]]},"references-count":78,"journal-issue":{"issue":"8006","published-print":{"date-parts":[[2024,4,4]]}},"alternative-id":["7155"],"URL":"https:\/\/doi.org\/10.1038\/s41586-024-07155-z","relation":{},"ISSN":["0028-0836","1476-4687"],"issn-type":[{"value":"0028-0836","type":"print"},{"value":"1476-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,6]]},"assertion":[{"value":"21 November 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 February 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 March 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}