Two Piwis with Ago-like functions silence somatic genes at the chromatin level

References

• Svoboda P. Introduction to RNAi and miRNA pathways. Nakladatelstv Karolinum. 2020
   Google Scholar
• Bhattacharjee S, Roche B, Martienssen RA. RNA-induced initiation of transcriptional silencing (RITS) complex structure and function. RNA Biol. 2019;16(9):1133–1146.
   PubMed Web of Science ®Google Scholar
• Yamashiro H, Siomi MC. PIWI-interacting RNA in Drosophila: biogenesis, transposon regulation, and beyond. Chem Rev. 2017;118(8):4404–4421.
   PubMed Web of Science ®Google Scholar
• Czech B, Munafò M, Ciabrelli F, et al. piRNA-guided genome defense: from biogenesis to silencing. Annu Rev Genet. 2018;52:131–157.
   PubMed Web of Science ®Google Scholar
• Weick EM, Miska EA. piRNAs: from biogenesis to function. Development. 2014;141(18):3458–3471.
   PubMed Web of Science ®Google Scholar
• Cenik ES, Zamore PD. Argonaute proteins. Curr Biol. 2011;21(12):R446–R449.
   PubMed Web of Science ®Google Scholar
• Stein CB, Genzor P, Mitra S, et al. Decoding the 5ʹ nucleotide bias of PIWI-interacting RNAs. Nat Commun. 2019;10(1):828.
   PubMedGoogle Scholar
• Parhad SS, Theurkauf WE. Rapid evolution and conserved function of the piRNA pathway. Royal Soc Open Biol. 2019;9(1):180181
   PubMed Web of Science ®Google Scholar
• Obbard DJ, Gordon KH, Buck AH, et al. The evolution of RNAi as a defence against viruses and transposable elements. Philos Trans R Soc B. 2009;364(1513):99–115.
   PubMed Web of Science ®Google Scholar
• Blumenstiel JP, Erwin AA, Hemmer LW. Focus: epigenetics: what Drives Positive Selection in the Drosophila piRNA Machinery? The Genomic Autoimmunity Hypothesis. Yale J Biol Med. 2016;89(4):499.
   PubMedGoogle Scholar
• Gu W, Shirayama M, Conte JD, et al. Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol cell. 2009;36(2):231–244.
   PubMed Web of Science ®Google Scholar
• Sarkies P, Selkirk ME, Jones JT, et al. Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages. PLoS Biol. 2015;13(2):e1002061.
   PubMed Web of Science ®Google Scholar
• Ross RJ, Weiner MM, Lin H. PIWI proteins and PIWI-interacting RNAs in the soma. Nature. 2014;505(7483):353.
   PubMed Web of Science ®Google Scholar
• Rojas-Ros P, Simonelig M. piRNAs and PIWI proteins: regulators of gene expression in development and stem cells. Development. 2018;145(17):dev161786.
   PubMed Web of Science ®Google Scholar
• Tosar JP, Rovira C, Cayota A. Non-coding RNA fragments account for the majority of annotated piRNAs expressed in somatic non-gonadal tissues. Commun Biol. 2018;1(1):1–8.
   PubMedGoogle Scholar
• Sarkar A, Volff JN, Vaury C. piRNAs and their diverse roles: a transposable element-driven tactic for gene regulation? FASEB J. 2017;31(2):436–446.
   PubMed Web of Science ®Google Scholar
• Lewis SH, Quarles KA, Yang Y, et al. Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements. Nat Ecol Evol. 2018;2(1):174–181.
   PubMed Web of Science ®Google Scholar
• Nekrasova IV, Potekhin AA. Diversity of RNA interference pathways in regulation of endogenous and exogenous sequences expression in ciliates Tetrahymena and Paramecium. Ecol Gene. 2019;17(2):113–125
   Google Scholar
• Bouhouche K, Gout JF, Kapusta A, et al. Functional specialization of Piwi proteins in Paramecium tetraurelia from post-transcriptional gene silencing to genome remodelling. Nucleic Acids Res. 2011;39(10):4249–4264.
   PubMed Web of Science ®Google Scholar
• Cheng CY, Orias E, Leu JY, et al. The evolution of germ–soma nuclear differentiation in eukaryotic unicells. Curr Biol. 2020;30(10):R502–R510.
   PubMed Web of Science ®Google Scholar
• Ruiz F, Vayssié L, Klotz C, et al. Homology-dependent gene silencing in Paramecium. Mol Biol Cell. 1998;9(4):931–943.
   PubMed Web of Science ®Google Scholar
• Götz U, Marker S, Cheaib M, et al. Two sets of RNAi components are required for heterochromatin formation in trans triggered by truncated transgenes. Nucleic Acids Res. 2016;44(12):5908–5923.
   PubMed Web of Science ®Google Scholar
• Rajeev Kumar S, Anunanthini P, Ramalingam S. Epigenetic silencing in transgenic plants. Front Plant Sci. 2015;6:693.
   PubMed Web of Science ®Google Scholar
• Hollick JB. Paramutation and related phenomena in diverse species. Nat Rev Genet. 2017;18(1):5.
   PubMed Web of Science ®Google Scholar
• Hermant C, Boivin A, Teysset L, et al. Paramutation in Drosophila requires both nuclear and cytoplasmic actors of the piRNA pathway and induces cis-spreading of piRNA production. Genetics. 2015;201(4):1381–1396.
   PubMed Web of Science ®Google Scholar
• Sapetschnig A, Sarkies P, Lehrbach NJ, et al. Tertiary siRNAs mediate paramutation in C. elegans. PLoS Genet. 2015;11(3):e1005078.
   PubMed Web of Science ®Google Scholar
• Galvani A, Sperling L. Transgene-mediated post-transcriptional gene silencing is inhibited by 3′ non-coding sequences in Paramecium. Nucleic Acids Res. 2001;29(21):4387–4394.
   PubMed Web of Science ®Google Scholar
• Garnier O, Serrano V, Duharcourt S, et al. RNA-mediated programming of developmental genome rearrangements in Paramecium tetraurelia. Mol Cell Biol. 2004;24(17):7370–7379.
   PubMed Web of Science ®Google Scholar
• De Vanssay A, Bougé AL, Boivin A, et al. Paramutation in Drosophila linked to emergence of a piRNA-producing locus. Nature. 2012;490(7418):112–115.
   PubMed Web of Science ®Google Scholar
• Lepere G, Nowacki M, Serrano V, et al. Silencing-associated and meiosis-specific small RNA pathways in Paramecium tetraurelia. Nucleic Acids Res. 2008;37(3):903–915.
   PubMed Web of Science ®Google Scholar
• Cheaib M, Dehghani Amirabad A, Nordström KJ, et al. Epigenetic regulation of serotype expression antagonizes transcriptome dynamics in Paramecium tetraurelia. DNA Res. 2015;22(4):293–305.
   PubMed Web of Science ®Google Scholar
• Simon MC, Marker S, Schmidt HJ. Inefficient serotype knock down leads to stable coexistence of different surface antigens on the outer membrane in Paramecium tetraurelia. Eur J Protistol. 2006;42(1):49–53.
   PubMed Web of Science ®Google Scholar
• Galvani A, Sperling L. RNA interference by feeding in Paramecium. Trends Genet. 2002;18(1):11–12.
   PubMed Web of Science ®Google Scholar
• Pirritano M, Götz U, Karunanithi S, et al. Environmental temperature controls accumulation of transacting siRNAs involved in heterochromatin formation. Genes (Basel). 2018;9(2):117.
   PubMed Web of Science ®Google Scholar
• Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–425.
   PubMed Web of Science ®Google Scholar
• Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. evolution. 1985;39(4):783–791.
   PubMed Web of Science ®Google Scholar
• Zuckerkandl E, Pauling L. Evolutionary divergence and convergence in proteins. In: Evolving genes and proteins.  New York: Elsevier; 1965. p. 97–166.
   Google Scholar
• Kumar S, Stecher G, Li M, et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547.
   PubMed Web of Science ®Google Scholar
• Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 2011;17(1):10–12.
   Google Scholar
• Karunanithi S, Simon M, Schulz MH. Automated analysis of small RNA datasets with RAPID. PeerJ. 2019;7:e6710.
   PubMed Web of Science ®Google Scholar
• Crooks GE, Hon G, Chandonia JM, et al. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188–1190.
   PubMed Web of Science ®Google Scholar
• Antoniewski C. Computing siRNA and piRNA overlap signatures. Methods Mol Biol. 2014;1173:135–146.
   PubMedGoogle Scholar
• Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
   PubMed Web of Science ®Google Scholar
• Klöppel C, Müller A, Marker S, et al. Two isoforms of eukaryotic phospholipase C in Paramecium affecting transport and release of GPI-anchored proteins in vivo. Eur J Cell Biol. 2009;88(10):577–592.
   PubMed Web of Science ®Google Scholar
• Frapporti A, Pina CM, Arnaiz O, et al. The Polycomb protein Ezl1 mediates H3K9 and H3K27 methylation to repress transposable elements in Paramecium. Nat Commun. 2019;10(1):1–15.
   PubMedGoogle Scholar
• Valentine MS, Rajendran A, Yano J, et al. Paramecium BBS genes are key to presence of channels in Cilia. Cilia. 2012;1(1):16.
   PubMedGoogle Scholar
• Preer LB, Hamilton G, Preer JRJR. Micronuclear DNA from Paramecium tetraurelia: serotype 51 A gene has internally eliminated sequences. J Protozool. 1992;39(6):678–682
   PubMedGoogle Scholar
• Furrer DI, Swart EC, Kraft MF, et al. Two sets of piwi proteins are involved in distinct sRNA pathways leading to elimination of Germline-Specific DNA. Cell Rep. 2017;20(2):505–520.
   PubMed Web of Science ®Google Scholar
• Aury JM, Jaillon O, Duret L, et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature. 2006;444(7116):171–178.
   PubMed Web of Science ®Google Scholar
• Arnaiz O, Sperling L. ParameciumDB in 2011: new tools and new data for functional and comparative genomics of the model ciliate Paramecium tetraurelia. Nucleic Acids Res. 2011;39(suppl_1):D632–D636.
   PubMedGoogle Scholar
• Jenkins BH, Maguire F, Leonard G, et al. Characterization of the RNA-interference pathway as a tool for reverse genetic analysis in the nascent phototrophic endosymbiosis, Paramecium bursaria. R Soc Open Sci. 2021;8(4):210140.
   PubMed Web of Science ®Google Scholar
• Nakanishi K, Ascano M, Gogakos T, et al. Eukaryote-specific insertion elements control human ARGONAUTE slicer activity. Cell Rep. 2013;3(6):1893–1900.
   PubMed Web of Science ®Google Scholar
• King BR, Vural S, Pandey S, et al. ngLOC: software and web server for predicting protein subcellular localization in prokaryotes and eukaryotes. BMC Res Notes. 2012;5(1):351.
   PubMedGoogle Scholar
• Carradec Q, Götz U, Arnaiz O, et al. Primary and secondary siRNA synthesis triggered by RNAs from food bacteria in the ciliate Paramecium tetraurelia. Nucleic Acids Res. 2015;43(3):1818–1833.
   PubMed Web of Science ®Google Scholar
• Karunanithi S, Oruganti V, Marker S, et al. Exogenous RNAi mechanisms contribute to transcriptome adaptation by phased siRNA clusters in Paramecium. Nucleic Acids Res. 2019;47(15):8036–8049.
   PubMed Web of Science ®Google Scholar
• Ji L, Chen X. Regulation of small RNA stability: methylation and beyond. Cell Res. 2012;22(4):624–636.
   PubMed Web of Science ®Google Scholar
• Sandoval PY, Swart EC, Arambasic M, et al. Functional diversification of Dicer-like proteins and small RNAs required for genome sculpting. Dev Cell. 2014;28(2):174–188.
   PubMed Web of Science ®Google Scholar
• Keeling PJ, Burger G, Durnford DG, et al. The tree of eukaryotes. Trends Ecol Evol. 2005;20(12):670–676.
   PubMed Web of Science ®Google Scholar
• Guang S, Bochner AF, Pavelec DM, et al. An Argonaute transports siRNAs from the cytoplasm to the nucleus. Science. 2008;321(5888):537–541.
   PubMed Web of Science ®Google Scholar
• Ye R, Wang W, Iki T, et al. Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol Cell. 2012;46(6):859–870.
   PubMed Web of Science ®Google Scholar
• Mi S, Cai T, Hu Y, et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5ʹ terminal nucleotide. Cell. 2008;133(1):116–127.
   PubMed Web of Science ®Google Scholar
• Brennecke J, Aravin AA, Stark A, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128(6):1089–1103.
   PubMed Web of Science ®Google Scholar
• Hoehener C, Hug I, Nowacki M. Dicer-like enzymes with sequence cleavage preferences. Cell. 2018;173(1):234–247.
   PubMed Web of Science ®Google Scholar
• Meijer HA, Smith EM, Bushell M. Regulation of miRNA strand selection: follow the leader? Biochem Soc Trans. 2014;42(4):1135–1140.
   PubMedGoogle Scholar
• Todesco M, Rubio-Somoza I, Paz-Ares J, et al. A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet. 2010;6(7). doi:10.1371/journal.pgen.1001031
   Web of Science ®Google Scholar
• Lee SR, Collins K. Physical and functional coupling of RNA-dependent RNA polymerase and Dicer in the biogenesis of endogenous siRNAs. Nat Struct Mol Biol. 2007;14(7):604–610.
   PubMed Web of Science ®Google Scholar
• Marasovico. Argonaute and Triman generate dicer-independent priRNAs and mature siRNAs to initiate heterochromatin formation. Mol Cell. 2013;52(2):173–183.
   PubMed Web of Science ®Google Scholar
• Wynant N, Santos D, Broeck JV. The evolution of animal Argonautes: evidence for the absence of antiviral AGO Argonautes in vertebrates. Sci Rep. 2017;7(1):1–13.
   PubMed Web of Science ®Google Scholar
• Maillard PV, Van der Veen AG, Deddouche-Grass S, et al. Inactivation of the type I interferon pathway reveals long double-stranded RNA-mediated RNA interference in mammalian cells. EMBO J. 2016;35(23):2505–2518.
   PubMed Web of Science ®Google Scholar
• Jinek M, Doudna JA. A three-dimensional view of the molecular machinery of RNA interference. Nature. 2009;457(7228):405–412.
   PubMed Web of Science ®Google Scholar