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Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements

Abstract

In animals, small RNA molecules termed PIWI-interacting RNAs (piRNAs) silence transposable elements (TEs), protecting the germline from genomic instability and mutation. piRNAs have been detected in the soma in a few animals, but these are believed to be specific adaptations of individual species. Here, we report that somatic piRNAs were probably present in the ancestral arthropod more than 500 million years ago. Analysis of 20 species across the arthropod phylum suggests that somatic piRNAs targeting TEs and messenger RNAs are common among arthropods. The presence of an RNA-dependent RNA polymerase in chelicerates (horseshoe crabs, spiders and scorpions) suggests that arthropods originally used a plant-like RNA interference mechanism to silence TEs. Our results call into question the view that the ancestral role of the piRNA pathway was to protect the germline and demonstrate that small RNA silencing pathways have been repurposed for both somatic and germline functions throughout arthropod evolution.

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Fig. 1: Genes in small RNA pathways evolve rapidly throughout the arthropods.
Fig. 2: piRNAs are absent in the B. terrestris male germline.
Fig. 3: Somatic piRNAs are widespread and target TEs throughout the arthropods.
Fig. 4: Virally derived small RNAs in three arthropod species.
Fig. 5: A model of the divergent small RNA pathways silencing TEs in different arthropods.

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References

  1. Aravin, A. A. et al. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 11, 1017–1027 (2001).

    Article  CAS  PubMed  Google Scholar 

  2. Aravin, A., Lagos-Quintana, M. & Yalcin, A. The small RNA profile during Drosophila melanogaster development. Dev. Cell 5, 337–350 (2003).

    Article  CAS  PubMed  Google Scholar 

  3. Czech, B. & Hannon, G. J. One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends Biochem. Sci. 41, 324–337 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Li, C. et al. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137, 509–521 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Malone, C. D. et al. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137, 522–535 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Morazzani, E. M., Wiley, M. R., Murreddu, M. G., Adelman, Z. N. & Myles, K. M. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog. 8, e1002470 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Miesen, P., Girardi, E. & van Rij, R. P. Distinct sets of piwi proteins produce arbovirus and transposon-derived piRNAs in Aedes aegypti mosquito cells. Nucleic Acids Res. 43, 6545–6556 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Jones, B. C. et al. A somatic piRNA pathway in the Drosophila fat body suppresses transposable elements ensuring metabolic homeostasis and normal lifespan. Nat. Commun. 7, 13856 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ghildiyal, M. et al. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320, 1077–1081 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Perrat, P. N. et al. Transposition-driven genomic heterogeneity in the Drosophila brain. Science 340, 91–95 (2013).

    Article  CAS  PubMed  Google Scholar 

  11. Palakodeti, D., Smielewska, M., Lu, Y.-C., Yeo, G. W. & Graveley, B. R. The piwi proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA 14, 1174–1186 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Reddien, P. W., Oviedo, N. J., Jennings, J. R., Jenkin, J. C. & Sánchez Alvarado, A. SMEDWI-2 is a piwi-like protein that regulates planarian stem cells. Science 310, 1327–1330 (2005).

    Article  CAS  PubMed  Google Scholar 

  13. Rajasethupathy, P. et al. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 149, 693–707 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Obbard, D. J., Gordon, K. H. J., Buck, A. H. & Jiggins, F. M. The evolution of RNAi as a defence against viruses and transposable elements. Phil. Trans. R. Soc. B 364, 99–115 (2009).

    Article  CAS  PubMed  Google Scholar 

  15. Kolaczkowski, B., Hupalo, D. N. & Kern, A. D. Recurrent adaptation in RNA interference genes across the Drosophila phylogeny. Mol. Biol. Evol. 28, 1033–1042 (2011).

    Article  CAS  PubMed  Google Scholar 

  16. Skinner, D. E., Rinaldi, G., Koziol, U., Brehm, K. & Brindley, P. J. How might flukes and tapeworms maintain genome integrity without a canonical piRNA pathway? Trends Parasitol. 30, 123–129 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Buck, A. H. & Blaxter, M. Functional diversification of Argonautes in nematodes: an expanding universe. Biochem. Soc. Trans. 41, 881–886 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Dowling, D. et al. Phylogenetic origin and diversification of RNAi pathway genes in insects. Genome Biol. Evol. 8, 3784–3793 (2017).

    Google Scholar 

  19. Lewis, S. H., Salmela, H. & Obbard, D. J. Duplication and diversification of Dipteran Argonaute genes, and the evolutionary divergence of Piwi and Aubergine. Genome Biol. Evol. 8, 507–518 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Palmer, W. J. & Jiggins, F. M. Comparative genomics reveals the origins and diversity of arthropod immune systems. Mol. Biol. Evol. 32, 2111–2129 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sarkar, A., Volff, J. N. & Vaury, C. piRNAs and their diverse roles: a transposable element-driven tactic for gene regulation? FASEB J. 31, 436–446 (2017).

    Article  CAS  PubMed  Google Scholar 

  22. Sarkies, P. et al. Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages. PLoS Biol. 13, e1002061 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tomoyasu, Y. et al. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol. 9, R10 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Campbell, C. L., Black, W. C., Hess, A. M. & Foy, B. D. Comparative genomics of small RNA regulatory pathway components in vector mosquitoes. BMC Genomics 9, 425 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Schiebel, W. et al. Isolation of an RNA-directed RNA polymerase-specific cDNA clone from tomato. Plant Cell 10, 2087–2102 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Zong, J., Yao, X., Yin, J., Zhang, D. & Ma, H. Evolution of the RNA-dependent RNA polymerase (RdRP) genes: duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 447, 29–39 (2009).

    Article  CAS  PubMed  Google Scholar 

  27. Bull, J. J. Advantage for the evolution of male. Heredity 43, 361–381 (1979).

    Article  Google Scholar 

  28. Robine, N. et al. A broadly conserved pathway generates 3′UTR-directed primary piRNAs. Curr. Biol. 19, 2066–2076 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Palatini, U. et al. Comparative genomics shows that viral integrations are abundant and express piRNAs in the arboviral vectors Aedes aegypti and Aedes albopictus. BMC Genomics 18, 512 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Alefelder, S., Patel, B. K. & Eckstein, F. Incorporation of terminal phosphorothioates into oligonucleotides. Nucleic Acids Res. 26, 4983–4988 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Zhang, Z., Theurkauf, W. E., Weng, Z. & Zamore, P. D. Strand-specific libraries for high throughput RNA sequencing (RNA-Seq) prepared without poly(A) selection. Silence 3, 9 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Han, B. W., Wang, W., Li, C. & Weng, Z. piRNA-guided transposon cleavage initiates Zucchini-dependent, phased piRNA production. Science 348, 817–821 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wickersheim, M. L. & Blumenstiel, J. P. Terminator oligo blocking efficiently eliminates rRNA from Drosophila small RNA sequencing libraries. Biotechniques 55, 269–272 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).

    Article  CAS  PubMed  Google Scholar 

  35. Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).

    Article  CAS  PubMed  Google Scholar 

  39. Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-4.0 (2013).

  40. Smit, A. F. A. & Hubley, R. RepeatModeler Open-1.0 (2008).

  41. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10 (2011).

    Article  Google Scholar 

  43. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Brennecke, J. et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128, 1089–1103 (2007).

    Article  CAS  PubMed  Google Scholar 

  46. Zhang, Z. et al. Heterotypic piRNA ping-pong requires Qin, a protein with both E3 ligase and Tudor domains. Mol. Cell 44, 572–584 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Antoniewski, C. in Animal Endo-siRNAs: Methods and Protocols (ed. Werner, A.) 135–146 (Humana, New York, 2014).

  48. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 15, 550 (2014).

    PubMed  PubMed Central  Google Scholar 

  50. Misof, B. et al. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767 (2014).

    Article  CAS  PubMed  Google Scholar 

  51. Giribet, G. & Edgecombe, G. D. Reevaluating the arthropod tree of life. Annu. Rev. Entomol. 57, 167–186 (2012).

    Article  CAS  PubMed  Google Scholar 

  52. Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  54. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank A. McGregor, D. Leite, M. Akam, R. Jenner, R. Kilner, A. Duarte, C. Jiggins, R. Wallbank, A. Bourke, T. Dalmay, N. Moran, K. Warchol, R. Callahan, G. Farley and T. Livdahl for providing the arthropods. H. Robertson provided the D. virgifera genome sequence. This research was supported by a Leverhulme Research Project Grant (RPG-2016-210 to F.M.J., E.A.M. and P.S.), a European Research Council grant (281668 DrosophilaInfection to F.M.J.), a Medical Research Council grant (MRC MC-A652-5PZ80 to P.S.), an Imperial College Research Fellowship (to P.S.), Cancer Research UK (C13474/A18583 and C6946/A14492 to E.A.M.), the Wellcome Trust (104640/Z/14/Z and 092096/Z/10/Z to E.A.M.) and a National Institutes of Health R37 grant (GM62862 to P.D.Z.).

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S.H.L. and K.A.Q. performed the experiments with assistance from Y.Y., M.T., L.F., S.A.S., P.P.S., R.C., C.G., I.G. and D.H.C. S.H.L., K.A.Q. and P.S. carried out the computational analysis. P.D.Z., E.A.M., P.S. and F.M.J. supervised the project. S.H.L., K.A.Q., P.D.Z., E.A.M., P.S. and F.M.J. wrote the paper.

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Correspondence to Samuel H. Lewis or Francis M. Jiggins.

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Lewis, S.H., Quarles, K.A., Yang, Y. et al. Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements. Nat Ecol Evol 2, 174–181 (2018). https://doi.org/10.1038/s41559-017-0403-4

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