RNA-Mediated Silencing in Eukaryotes: Evolution of Protein Components and Biological Roles

  • J. Armando Casas-MollanoEmail author
  • Ericka Zacarias
  • Xinrong Ma
  • Eun-Jeong Kim
  • Heriberto CeruttiEmail author


RNA interference (RNAi), the process by which small RNAs (~20–30 nt in length) derived from double-stranded RNA precursors can induce silencing of cognate sequences, was initially characterized in Caenorhabditis elegans. Since then distinct RNAi mechanisms and pathways have been described in diverse eukaryotes, suggesting that RNA-mediated silencing is an evolutionary conserved process in the eukaryotic domain of life. Core protein components of the RNAi machinery include Argonaute-PIWI polypeptides, RNAseIII-like endonucleases termed Dicers and RNA-dependent RNA polymerases. Although the archetypal domains of these proteins appear to have been assembled from prokaryotic sources, phylogenetic analyses indicate that the three components came together as a functional unit in the last common ancestor of eukaryotes. Consistent with this interpretation, core RNAi proteins are widely distributed among organisms in all major eukaryotic lineages, particularly Argonaute-PIWI polypeptides, which typify the key RNAi players. Nonetheless, the RNAi machinery has also been lost independently in multiple divergent species during evolution, suggesting that its ancestral function was not essential for unicellular life. The prevailing hypothesis is that the primeval RNAi machinery emerged as a defense system against parasitic genetic elements such as viruses and transposons. In contrast, a regulatory function of RNAi, through microRNAs and an assortment of other distinct small RNAs, may have evolved more recently, influencing newly arisen, lineage-specific processes such as cell differentiation and development in multicellular eukaryotes. However, defining the contribution of small RNA-mediated gene regulation to the evolution of organismal complexity remains a challenge for the future.


Eukaryotic Lineage RNAi Machinery Eukaryotic Evolution PIWI Protein PIWI Domain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



JAC-M is supported by a Young Investigator grant from the São Paulo Research Foundation (FAPESP 2011/50483-2). This work was supported in part by a grant from the National Science Foundation (to HC). We apologize to all researchers whose contributions could not be cited because of space limitations.


  1. 1.
    Cerutti H, Ma X, Msanne J, Repas T. RNA-mediated silencing in Algae: biological roles and tools for analysis of gene function. Eukaryot Cell. 2011;10:1164–72. doi: 10.1128/EC.05106-11.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Poulsen C, Vaucheret H, Brodersen P. Lessons on RNA silencing mechanisms in plants from eukaryotic argonaute structures. Plant Cell. 2013;25:22–37. doi: 10.1105/tpc.112.105643.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Swarts DC, Makarova K, Wang Y, Nakanishi K, Ketting RF, Koonin EV, Patel DJ, van der Oost J. The evolutionary journey of Argonaute proteins. Nat Struct Mol Biol. 2014;21:743–53. doi: 10.1038/nsmb.2879.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Borges F, Martienssen RA. The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol. 2015;16:727–41. doi: 10.1038/nrm4085.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Ipsaro JJ, Joshua-Tor L. From guide to target: molecular insights into eukaryotic RNA-interference machinery. Nat Struct Mol Biol. 2015;22:20–8. doi: 10.1038/nsmb.2931.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Iwakawa HO, Tomari Y. The functions of microRNAs: mRNA decay and translational repression. Trends Cell Biol. 2015;25:651–65. doi: 10.1016/j.tcb.2015.07.011.CrossRefPubMedGoogle Scholar
  7. 7.
    Jonas S, Izaurralde E. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet. 2015;16:421–33. doi: 10.1038/nrg3965.CrossRefPubMedGoogle Scholar
  8. 8.
    Leung AK. The whereabouts of microRNA actions: cytoplasm and beyond. Trends Cell Biol. 2015;25:601–10. doi: 10.1016/j.tcb.2015.07.005.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Wilczynska A, Bushell M. The complexity of miRNA-mediated repression. Cell Death Differ. 2015;22:22–33. doi: 10.1038/cdd.2014.112.CrossRefPubMedGoogle Scholar
  10. 10.
    Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391:806–11. doi: 10.1038/35888.CrossRefPubMedGoogle Scholar
  11. 11.
    Chu Y, Yue X, Younger ST, Janowski BA, Corey DR. Involvement of argonaute proteins in gene silencing and activation by RNAs complementary to a non-coding transcript at the progesterone receptor promoter. Nucleic Acids Res. 2010;38:7736–48. doi: 10.1093/nar/gkq648.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Mortensen RD, Serra M, Steitz JA, Vasudevan S. Posttranscriptional activation of gene expression in Xenopus laevis oocytes by microRNA-protein complexes (microRNPs). Proc Natl Acad Sci USA. 2011;108:8281–6. doi: 10.1073/pnas.1105401108.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Gagnon KT, Li L, Chu Y, Janowski BA, Corey DR. RNAi factors are present and active in human cell nuclei. Cell Rep. 2014;6:211–21. doi: 10.1016/j.celrep.2013.12.013.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Guo D, Barry L, Lin SS, Huang V, Li LC. RNAa in action: from the exception to the norm. RNA Biol. 2014;11:1221–5. doi: 10.4161/15476286.2014.972853.CrossRefPubMedGoogle Scholar
  15. 15.
    Burroughs AM, Ando Y, Aravind L. New perspectives on the diversification of the RNA interference system: insights from comparative genomics and small RNA sequencing. Wiley Interdiscip Rev RNA. 2014;5:141–81. doi: 10.1002/wrna.1210.CrossRefPubMedGoogle Scholar
  16. 16.
    Peng JC, Lin H. Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism. Curr Opin Cell Biol. 2013;25:190–4. doi: 10.1016/ Scholar
  17. 17.
    Dueck A, Meister G. Assembly and function of small RNA—argonaute protein complexes. Biol Chem. 2014;395:611–29. doi: 10.1515/hsz-2014-0116.CrossRefPubMedGoogle Scholar
  18. 18.
    Schirle NT, MacRae IJ. The crystal structure of human Argonaute2. Science. 2012;336:1037–40. doi: 10.1126/science.1221551.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Sasaki HM, Tomari Y. The true core of RNA silencing revealed. Nat Struct Mol Biol. 2012;19:657–60. doi: 10.1038/nsmb.2302.CrossRefPubMedGoogle Scholar
  20. 20.
    Faehnle CR, Elkayam E, Haase AD, Hannon GJ, Joshua-Tor L. The making of a slicer: activation of human Argonaute-1. Cell Rep. 2013;3:1901–9. doi: 10.1016/j.celrep.2013.05.033.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Hauptmann J, Dueck A, Harlander S, Pfaff J, Merkl R, Meister G. Turning catalytically inactive human Argonaute proteins into active slicer enzymes. Nat Struct Mol Biol. 2013;20:814–7. doi: 10.1038/nsmb.2577.CrossRefPubMedGoogle Scholar
  22. 22.
    Nakanishi K, Ascano M, Gogakos T, Ishibe-Murakami S, Serganov AA, Briskin D, Morozov P, Tuschl T, Patel DJ. Eukaryote-specific insertion elements control human Argonaute slicer activity. Cell Rep. 2013;3:1893–900. doi: 10.1016/j.celrep.2013.06.010.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Sheng G, Zhao H, Wang J, Rao Y, Tian W, Swarts DC, van der Oost J, Patel DJ, Wang Y. Structure-based cleavage mechanism of Thermus thermophilus Argonaute DNA guide strand-mediated DNA target cleavage. Proc Natl Acad Sci USA. 2014;111:652–7. doi: 10.1073/pnas.1321032111.CrossRefPubMedGoogle Scholar
  24. 24.
    Baulcombe D. RNA silencing in plants. Nature. 2004;431:356–63. doi: 10.1038/nature02874.CrossRefPubMedGoogle Scholar
  25. 25.
    Cerutti H, Casas-Mollano JA. On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet. 2006;50:81–99. doi: 10.1007/s00294-006-0078-x.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–33. doi: 10.1016/j.cell.2009.01.002.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Dang Y, Yang Q, Xue Z, Liu Y. RNA interference in fungi: pathways, functions, and applications. Eukaryot Cell. 2011;10:1148–55. doi: 10.1128/EC.05109-11.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Billmyre RB, Calo S, Feretzaki M, Wang X, Heitman J. RNAi function, diversity, and loss in the fungal kingdom. Chromosome Res. 2013;21:561–72. doi: 10.1007/s10577-013-9388-2.CrossRefPubMedGoogle Scholar
  29. 29.
    Nicolas FE, Torres-Martinez S, Ruiz-Vazquez RM. Loss and retention of RNA interference in fungi and parasites. PLoS Pathog. 2013;9:e1003089. doi: 10.1371/journal.ppat.1003089.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Hoogstrate SW, Volkers RJ, Sterken MG, Kammenga JE, Snoek LB. Nematode endogenous small RNA pathways. Worm. 2014;3:e28234. doi: 10.4161/worm.28234.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Posadas DM, Carthew RW. MicroRNAs and their roles in developmental canalization. Curr Opin Genet Dev. 2014;27:1–6. doi: 10.1016/j.gde.2014.03.005.CrossRefPubMedGoogle Scholar
  32. 32.
    Gebert D, Rosenkranz D. RNA-based regulation of transposon expression. Wiley Interdiscip Rev RNA. 2015;6:687–708. doi: 10.1002/wrna.1310.CrossRefPubMedGoogle Scholar
  33. 33.
    Malone CD, Hannon GJ. Small RNAs as guardians of the genome. Cell. 2009;136:656–68. doi: 10.1016/j.cell.2009.01.045.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Axtell MJ, Westholm JO, Lai EC. Vive la difference: biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 2011;12:221. doi: 10.1186/gb-2011-12-4-221.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Ishizu H, Siomi H, Siomi MC. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 2012;26:2361–73. doi: 10.1101/gad.203786.112.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Rogers K, Chen X. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell. 2013;25:2383–99. doi: 10.1105/tpc.113.113159.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Ketting RF. The many faces of RNAi. Dev Cell. 2011;20:148–61. doi: 10.1016/j.devcel.2011.01.012.CrossRefPubMedGoogle Scholar
  38. 38.
    Shabalina SA, Koonin EV. Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol. 2008;23:578–87. doi: 10.1016/j.tree.2008.06.005.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Mukherjee K, Campos H, Kolaczkowski B. Evolution of animal and plant dicers: early parallel duplications and recurrent adaptation of antiviral RNA binding in plants. Mol Biol Evol. 2013;30:627–41. doi: 10.1093/molbev/mss263.CrossRefPubMedGoogle Scholar
  40. 40.
    Letunic I, Doerks T, Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 2015;43:D257–60. doi: 10.1093/nar/gku949.CrossRefPubMedGoogle Scholar
  41. 41.
    Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44:D279–85. doi: 10.1093/nar/gkv1344.CrossRefPubMedGoogle Scholar
  42. 42.
    Nakanishi K, Weinberg DE, Bartel DP, Patel DJ. Structure of yeast Argonaute with guide RNA. Nature. 2012;486:368–74. doi: 10.1038/nature11211.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Burroughs AM, Iyer LM, Aravind L. Two novel PIWI families: roles in inter-genomic conflicts in bacteria and Mediator-dependent modulation of transcription in eukaryotes. Biol Direct. 2013;8:13. doi: 10.1186/1745-6150-8-13.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Aravind L, Walker DR, Koonin EV. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 1999;27:1223–42.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Makarova KS, Wolf YI, Koonin EV. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res. 2013;41:4360–77. doi: 10.1093/nar/gkt157.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Makarova KS, Wolf YI, van der Oost J, Koonin EV. Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol Direct. 2009;4:29. doi: 10.1186/1745-6150-4-29.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Hock J, Meister G. The Argonaute protein family. Genome Biol. 2008;9:210. doi: 10.1186/gb-2008-9-2-210.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Pak J, Fire A. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science. 2007; 315:241–244. doi: 10.1126/science.1132839.Google Scholar
  49. 49.
    Sijen T, Steiner FA, Thijssen KL, Plasterk RH. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science. 2007;315:244–7. doi: 10.1126/science.1136699.CrossRefPubMedGoogle Scholar
  50. 50.
    Wedeles CJ, Wu MZ, Claycomb JM. Protection of germline gene expression by the C. elegans Argonaute CSR-1. Dev Cell. 2013;27:664–71. doi: 10.1016/j.devcel.2013.11.016.CrossRefPubMedGoogle Scholar
  51. 51.
    Meister G. Argonaute proteins: functional insights and emerging roles. Nat Rev Genet. 2013;14:447–59. doi: 10.1038/nrg3462.CrossRefPubMedGoogle Scholar
  52. 52.
    Swart EC, Nowacki M. The eukaryotic way to defend and edit genomes by sRNA-targeted DNA deletion. Ann NY Acad Sci. 2015;1341:106–14. doi: 10.1111/nyas.12636.CrossRefPubMedGoogle Scholar
  53. 53.
    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–8. doi: 10.1093/bioinformatics/btm404.CrossRefPubMedGoogle Scholar
  54. 54.
    Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.PubMedGoogle Scholar
  55. 55.
    Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007;24:1596–9. doi: 10.1093/molbev/msm092.CrossRefPubMedGoogle Scholar
  56. 56.
    Macrae IJ, Zhou K, Li F, Repic A, Brooks AN, Cande WZ, Adams PD, Doudna JA. Structural basis for double-stranded RNA processing by Dicer. Science. 2006;311:195–8. doi: 10.1126/science.1121638.CrossRefPubMedGoogle Scholar
  57. 57.
    Patrick KL, Shi H, Kolev NG, Ersfeld K, Tschudi C, Ullu E. Distinct and overlapping roles for two Dicer-like proteins in the RNA interference pathways of the ancient eukaryote Trypanosoma brucei. Proc Natl Acad Sci USA. 2009;106:17933–8. doi: 10.1073/pnas.0907766106.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W. Single processing center models for human Dicer and bacterial RNase III. Cell. 2004;118:57–68. doi: 10.1016/j.cell.2004.06.017.CrossRefPubMedGoogle Scholar
  59. 59.
    Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH, Fink GR, Bartel DP. RNAi in budding yeast. Science. 2009;326:544–50. doi: 10.1126/science.1176945.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Weinberg DE, Nakanishi K, Patel DJ, Bartel DP. The inside-out mechanism of Dicers from budding yeasts. Cell. 2011;146:262–76. doi: 10.1016/j.cell.2011.06.021.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Shi H, Tschudi C, Ullu E. An unusual Dicer-like1 protein fuels the RNA interference pathway in Trypanosoma brucei. RNA. 2006;12:2063–72. doi: 10.1261/rna.246906.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Hu Y, Stenlid J, Elfstrand M, Olson A. Evolution of RNA interference proteins dicer and argonaute in Basidiomycota. Mycologia. 2013;105:1489–98. doi: 10.3852/13-171.CrossRefPubMedGoogle Scholar
  63. 63.
    Sandoval PY, Swart EC, Arambasic M, Nowacki M. Functional diversification of Dicer-like proteins and small RNAs required for genome sculpting. Dev Cell. 2014;28:174–88. doi: 10.1016/j.devcel.2013.12.010.CrossRefPubMedGoogle Scholar
  64. 64.
    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. 2009;447:29–39. doi: 10.1016/j.gene.2009.07.004.CrossRefPubMedGoogle Scholar
  65. 65.
    Hammond TM, Keller NP. RNA silencing in Aspergillus nidulans is independent of RNA-dependent RNA polymerases. Genetics. 2005;169:607–17. doi: 10.1534/genetics.104.035964.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Yang JS, Lai EC. Dicer-independent, Ago2-mediated microRNA biogenesis in vertebrates. Cell Cycle. 2010;9:4455–60.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Yang JS, Maurin T, Lai EC. Functional parameters of Dicer-independent microRNA biogenesis. RNA. 2012;18:945–57. doi: 10.1261/rna.032938.112.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Olovnikov I, Chan K, Sachidanandam R, Newman DK, Aravin AA. Bacterial argonaute samples the transcriptome to identify foreign DNA. Mol Cell. 2013;51:594–605. doi: 10.1016/j.molcel.2013.08.014.CrossRefPubMedGoogle Scholar
  69. 69.
    Swarts DC, Jore MM, Westra ER, Zhu Y, Janssen JH, Snijders AP, Wang Y, Patel DJ, Berenguer J, Brouns SJ, van der Oost J. DNA-guided DNA interference by a prokaryotic Argonaute. Nature. 2014;507:258–61. doi: 10.1038/nature12971.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Zander A, Holzmeister P, Klose D, Tinnefeld P, Grohmann D. Single-molecule FRET supports the two-state model of Argonaute action. RNA Biol. 2014;11:45–56. doi: 10.4161/rna.27446.CrossRefPubMedGoogle Scholar
  71. 71.
    Ma X, Kim EJ, Kook I, Ma F, Voshall A, Moriyama E, Cerutti H. Small interfering RNA-mediated translation repression alters ribosome sensitivity to inhibition by cycloheximide in Chlamydomonas reinhardtii. Plant Cell. 2013;25:985–98. doi: 10.1105/tpc.113.109256.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 2005;19:489–501. doi: 10.1101/gad.1248505.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Martienssen RA, Zaratiegui M, Goto DB. RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe. Trends Genet. 2005;21:450–6. doi: 10.1016/j.tig.2005.06.005.CrossRefPubMedGoogle Scholar
  74. 74.
    Casas-Mollano JA, Rohr J, Kim EJ, Balassa E, van Dijk K, Cerutti H. Diversification of the core RNA interference machinery in Chlamydomonas reinhardtii and the role of DCL1 in transposon silencing. Genetics. 2008;179:69–81. doi: 10.1534/genetics.107.086546.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Wang X, Hsueh YP, Li W, Floyd A, Skalsky R, Heitman J. Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev. 2010;24:2566–82. doi: 10.1101/gad.1970910.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Nakayashiki H, Kadotani N, Mayama S. Evolution and diversification of RNA silencing proteins in fungi. J Mol Evol. 2006;63:127–35. doi: 10.1007/s00239-005-0257-2.CrossRefPubMedGoogle Scholar
  77. 77.
    Berezikov E. Evolution of microRNA diversity and regulation in animals. Nat Rev Genet. 2011;12:846–60. doi: 10.1038/nrg3079.CrossRefPubMedGoogle Scholar
  78. 78.
    Drinnenberg IA, Fink GR, Bartel DP. Compatibility with killer explains the rise of RNAi-deficient fungi. Science. 2011;333:1592. doi: 10.1126/science.1209575.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Voshall A, Kim EJ, Ma X, Moriyama EN, Cerutti H. Identification of AGO3-associated miRNAs and computational prediction of their targets in the green alga Chlamydomonas reinhardtii. Genetics. 2015;200:105–21. doi: 10.1534/genetics.115.174797.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Yamasaki T, Kim EJ, Cerutti H, Ohama T. Argonaute3 is a key player in miRNA-mediated target cleavage and translational repression in Chlamydomonas. Plant J. 2015;. doi: 10.1111/tpj.13107.Google Scholar
  81. 81.
    Smialowska A, Djupedal I, Wang J, Kylsten P, Swoboda P, Ekwall K. RNAi mediates post-transcriptional repression of gene expression in fission yeast Schizosaccharomyces pombe. Biochem Biophys Res Commun. 2014;444:254–9. doi: 10.1016/j.bbrc.2014.01.057.CrossRefPubMedGoogle Scholar
  82. 82.
    Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature. 2008;455:1193–7. doi: 10.1038/nature07415.CrossRefPubMedGoogle Scholar
  83. 83.
    Cuperus JT, Fahlgren N, Carrington JC. Evolution and functional diversification of MIRNA genes. Plant Cell. 2011;23:431–42. doi: 10.1105/tpc.110.082784.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Lenz D, May P, Walther D. Comparative analysis of miRNAs and their targets across four plant species. BMC Res Notes. 2011;4:483. doi: 10.1186/1756-0500-4-483.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Sheng Y, Previti C. Genomic features and computational identification of human microRNAs under long-range developmental regulation. BMC Genom. 2011;12:270. doi: 10.1186/1471-2164-12-270.CrossRefGoogle Scholar
  86. 86.
    Nozawa M, Miura S, Nei M. Origins and evolution of microRNA genes in plant species. Genome Biol Evol. 2012;4:230–9. doi: 10.1093/gbe/evs002.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Tarver JE, Donoghue PC, Peterson KJ. Do miRNAs have a deep evolutionary history? BioEssays. 2012;34:857–66. doi: 10.1002/bies.201200055.CrossRefPubMedGoogle Scholar
  88. 88.
    Tarver JE, Cormier A, Pinzon N, Taylor RS, Carre W, Strittmatter M, Seitz H, Coelho SM, Cock JM. microRNAs and the evolution of complex multicellularity: identification of a large, diverse complement of microRNAs in the brown alga Ectocarpus. Nucleic Acids Res. 2015;43:6384–98. doi: 10.1093/nar/gkv578.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Departamento de Bioquímica, Instituto de QuímicaUniversidade de São PauloSão PauloBrazil
  2. 2.School of Biological Sciences and Center for Plant Science InnovationUniversity of Nebraska-LincolnLincolnUSA

Personalised recommendations